research studies on pressure ulcer prevention

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• Volume 11, Issue 3
• Effects of implementing Pressure Ulcer Prevention Practice Guidelines (PUPPG) in the prevention of pressure ulcers among hospitalised elderly patients: a systematic review protocol
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• Amos Wung Buh 1 ,
• Hassan Mahmoud 2 ,
• http://orcid.org/0000-0001-5398-8508 Wenjun Chen 3 , 4 ,
• Matthew D F McInnes 2 , 5 , 6 ,
• http://orcid.org/0000-0002-3389-2485 Dean A Fergusson 6
• 1 Interdisciplinary School of Health Sciences , University of Ottawa , Ottawa , Ontario , Canada
• 2 School of Epidemiology and Public Health, Faculty of Medicine , University of Ottawa , Ottawa , Ontario , Canada
• 3 School of Nursing , University of Ottawa , Ottawa , Ontario , Canada
• 4 Xiangya School of Nursing , Central South University , Changsha , Hunan , China
• 5 Department of Radiology , University of Ottawa , Ottawa , Ontario , Canada
• 6 Clinical Epidemiology Program , Ottawa Hospital Research Institute , Ottawa , Ontario , Canada
• Correspondence to Wenjun Chen; wchen140{at}uottawa.ca

Introduction Pressure ulcers are serious and potentially life-threatening problems across all age groups and across all medical specialties and care settings. The hospitalised elderly population is the most common group to develop pressure ulcers. This study aims to systematically review studies implementing pressure ulcer prevention strategies recommended in the Pressure Ulcer Prevention Practice Guidelines for the prevention of pressure ulcers among hospitalised elderly patients globally.

Methods and analysis A systematic review of all studies that have assessed the use of pressure ulcer prevention strategies in hospital settings among hospitalised elderly patients shall be conducted. A comprehensive search of all published articles in Medline Ovid, Cumulative Index to Nursing and Allied Health Literature, PubMed, Embase, Cochrane library, Scopus and Web of Science will be done using terms such as pressure ulcers, prevention strategies, elderly patients and hospital. Studies will be screened for eligibility through title, abstract and full text by two independent reviewers. Study quality and risk of bias will be assessed using the Joanna Briggs Institute for Meta-Analysis of Statistics Assessment and Review Instrument. If sufficient data are available, a meta-analysis will be conducted to synthesise the effect size reported as OR with 95% CIs using both fixed and random effect models. I 2 statistics and visual inspection of the forest plots will be used to assess heterogeneity and identify the potential sources of heterogeneity. Publication bias will be assessed by visual inspections of funnel plots and Egger’s test.

Ethics and dissemination No formal ethical approval or consent is required as no primary data will be collected. We aim to publish the research findings in a peer-reviewed scientific journal to promote knowledge transfer, as well as in conferences, seminars, congresses or symposia in a traditional manner.

PROSPERO registration number CRD42019129088.

• geriatric dermatology
• geriatric medicine
• protocols & guidelines
• orthopaedic & trauma surgery
• wound management

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See:  http://creativecommons.org/licenses/by-nc/4.0/ .

https://doi.org/10.1136/bmjopen-2020-043042

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Strengths and limitations of this study

This is a systematic review and meta-analysis of randomised controlled trials.

This review will be the first to synthesise the evidence regarding the effectiveness of guidelines used in pressure ulcer prevention for elderly patients in hospitals and offer the highest level of evidence for informed decisions on use of Pressure Ulcer Prevention Practice Guidelines (PUPPG) in prevention pressure ulcers in the elderly patients in hospital.

There may be heterogeneity of interventions used on eligible studies and incomplete information reported about the interventions in the literature which could limit our ability to statistically compare the effectiveness of interventions.

The main limitation of this review might be scarcity of randomised controlled trials on the use of PUPPG for preventing pressure ulcers in elderly patients, publication bias and methodological quality of grey literature that shall be found.

Pressure ulcers (PU) also known as pressure injuries are areas of localised damage to the skin and/or underlying structures due to pressure and/or friction and shear. 1 They are serious and potentially life-threatening problems across all age groups from the very young to the very old and across all medical specialties and care settings. 2 It has been documented that hospital admissions due to PU are 75% higher than admissions for any other medical conditions and that, the consequences of PU development in hospitalised patients are particularly serious. 2 Patients with hospital admission PU are three times more likely to be discharged to long-term care facilities and mortality of these patients is twice that of patients without hospital admission PU. 3 The cost of treatment of PU is 2.5 times than its prevention, and PU increases the length of stay in the hospital from 4 to 30 days, decreases quality of life, and increases pain, morbidity and mortality. 4

On international level, hospital-acquired PUs (sometimes called decubitus ulcers) are very common. 5 Although many of these cases are preventable, their point prevalence in Canadian hospitals for example is measured to be 25.1%. 6 Unfortunately, the high rates of such condition are associated with subsequent high burden on the healthcare system and the national economy considering the high cost of their management, and the frequent occurrence of associated significant morbidity and mortality. 5 According to the Ontario Case Costing Initiative database in 2013 using the European Pressure Ulcer Advisory Panel (EPUAP) staging system, it was estimated that the cost of management of stage II ulcer is up to US$40 000 and can reach more than double this price for managing a single case of stage IV ulcer. 7 A good example of the burden that PU add to the national economy was measured in USA; it was estimated that hospital acquired PUs increase the financial expenses on healthcare systems between US$6 and US$15 billion annually. 8

The National Pressure Ulcer Advisory Panel (NPUAP), the EPUAP and the Pan Pacific Pressure Injury Alliance (PPPIA) 9 have defined PU as a ‘lesion or a trauma to the skin and/or underlying tissue usually over a bony prominence and is the result of undiminished pressure, or pressure combination with shear, friction and moisture’. It is a degenerative progress attributable to biological tissues (skin and underlying tissues) being exposed to pressure and shearing forces. The pressure constrains the proper blood circulation and causes cell death, tissue necrosis and the development of ulcers. 9 While the quality of PU prevention and treatment has increased considerably over the past years, PUs remains a global concern because of its frequency of occurrence and negative consequences for patients and families as well as for the healthcare system. 10 Incidence of PUs for hospitalised patients ranges from 9% to 18%, among which the elderly population appears to be the most common group to develop the ulcers. 11 At the same time, many elderly patients are more vulnerable to be ‘stuck’ at a certain stage of PU for a long period of time and sometimes for the remainder of their lives. 12 This may result in longer length of hospital stay, heavier burdens for the healthcare system and family members, worst quality of life for elderly patients, which may also influence their mental health such as emotional stability. 13 14

NPUAP, EPUAP and PPPIA 9 developed the Pressure Ulcer Prevention Practice Guideline (PUPPG), which involves a range of evidence-based recommendations for PUs prevention that could be applied by healthcare professionals globally. Frequently used PU prevention strategies recommended in this guideline includes PU risk assessment, regular repositioning, prevention management plan, appropriate use of support surfaces and protection, continence management, patient education, skin protection, nutritional assessment and adequate nutrition. 15 It also includes some recommendations specifically for elderly people—‘protect aged skin from skin injury associated with pressure and shear forces’, taking into consideration that an aged person’s skin is vulnerable. 15

A number of studies have been conducted on the implementation of PU prevention strategies among hospitalised patients. One cluster randomised trial conducted in Canada revealed that multidisciplinary PU prevention groups are more cost effective than usual care and yields no significant improvement in the treatment of PUs. 16 Despite the existence of the guidelines on the prevention of PU, their effective utilisation in preventing PUs among hospitalised elderly patients varies in settings and countries. Also, although a number of studies have assessed strategies used in preventing PUs, there appears to be little or no information on systematic reviews that have assessed the effectiveness of guidelines used in PU prevention for elderly patients in hospitals. This study, therefore, aims to systematically review studies implementing PU prevention strategies recommended in the PUPPG for the prevention of PUs among hospitalised elderly patients globally.

The objective of this review is to assess the effectiveness of each of the strategies included in the PUPPG guideline in reducing the incidence and prevalence of hospital acquired PUs in hospitalised elderly patients in comparison to no strategy (usual practice), or other strategies. The review question is: what is the effectiveness of implementing each of the PU prevention strategies included in the PUPPG in decreasing the incidence and prevalence of PUs among hospitalised elderly patients compared with no strategies (basic usual care) or different prevention strategies?

Study design

This will be a systematic review and meta-analysis of published and unpublished studies that have assessed the use of PU prevention strategies in hospital settings among hospitalised elderly patients. The systematic review protocol has been developed and reported following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) criteria (see online supplemental appendix 1 ). 17

Supplemental material

Inclusion criteria, population included.

This systematic review will focus on studies that involved all vitally stable (not admitted in the intensive care unit) bed ridden hospitalised patients aged 60 or above.

Interventions

All studies that assessed the effect of PU preventive strategies found in the PUPPG, that were implemented on vitally stable bed ridden hospitalised patients aged 60 and above with an aim to decrease the occurrence of PUs, will be included in this review. Interventions will be limited to use of risk assessment, skin assessment, skin care, nutrition, position and repositioning, education and training, and medical devices care.

Interventions will be compared with other strategies to identify the most effective among them and/or will also be compared with no interventions (regular basic management).

In this study, the primary outcome will be directly related to the incidence of the disease among elderly hospitalised patients (incidence shall be considered as the proportion of hospitalised patients who developed PUs while in hospital). Included studies must measure study duration related incidence of the disease and/or its point prevalence and /or stage of PU (severity) as a measure of the effectiveness of the preventive strategies.

Types of studies

We will focus only on Quantitative studies—experimental and quasi-experimental studies. These might include randomised and non-randomised controlled trials in addition to comparative and before-and-after studies.

Only studies written in English will be included in this systematic review.

Search strategy

We will use a three-step strategy to find published and unpublished studies on PUs and their management. First, we will conduct an initial search through the Medline Ovid database using an analysis of text words found in the title and abstract, and the index terms used to describe the article. Second, we will use identified keywords and index terms to search for studies in identified databases. Finally, we will use the reference list of selected studies from the first and second searches to look for additional studies not found in the databases. For this study, we will consider only studies either published or unpublished in English.

The databases that shall be searched for this review will include Medline Ovid, Cumulative Index to Nursing and Allied Health Literature, PubMed, Embase, Cochrane library, Scopus and Web of Science. See online supplemental appendix 2 for the example searching strategy and results in Medline (Ovid). All these databases will provide published studies. To find unpublished studies on our topic, we will use Google, Grey Literature reports and the Centers for Disease Control and Prevention.

The keywords we will use for our initial searches in Medline Ovid will include ‘pressure ulcers’, ‘pressure sore’, ‘bed sore’, ‘pressure injuries’, ‘prevention strategies’, ‘elderly patients’ and ‘hospital’.

Study screening and selection

The titles, abstracts and full text of studies selected for this study will be reviewed by two independent researchers to identify studies that potentially meet the inclusion criteria outlined above. The Covidence software will be used for title, abstract and full-text screening. After importing references and inclusion/exclusion criteria into the Covidence software, two independent reviewers will screen titles of included studies according to the eligible criteria. Conflicts between those two reviewers will be resolved through discussion with a third reviewer. The same procedures shall be used for abstract screening. Following the abstract screening, full texts of these potentially eligible studies will be retrieved and independently assessed for eligibility by two reviewers. Any disagreement between the two reviewers over the eligibility of a particular study will also be resolved through discussion with the third reviewer. The process of study selection will be reported using the PRISMA flow diagram. 17

Assessment of methodological quality

Two independent reviewers will be used to assess the methodological validity of the quantitative papers that will be selected for retrieval prior to their inclusion in the review using standard critical appraisal tools from the Joanna Briggs Institute for Meta-Analysis of Statistics Assessment and Review Instrument (see online supplemental appendix 3 ). All disagreement between the two reviewers shall be settled through discussions.

Data extraction

After screening and selecting studies, key information from those studies will be extracted into an excel sheet for further analysis. We shall use a data extraction tool adapted from the standardised data extraction tool from the Joanna Briggs Institute Meta-Analysis of Statistics Assessment and Review Instrument (JBI-MAStARI). Considering the information, we will need for the data synthesis of our study, we shall use the JBI-MAStARI to develop a data extraction tool specifically for quantitative research data extraction (see online supplemental appendix 4 ). The tool will be used to extract: (1) Study characteristics of reviewed papers, such as authors, year of publication, journal; (2) Methods of the study, including study design (randomised control trial (RCT), quasi-RCT, longitudinal, retrospective), research purpose and/or questions; (3) participant characteristics, country where the study took place, setting, population, sample size, age, sex, ethnicity, socioeconomic status and/or education level; (4) PU prevention strategies used in experimental group and control group (if applicable), (5) outcome measures and results and (6) conclusions of reviewed papers and any comments from reviewers. Two reviewers will independently perform data extraction. Authors of reviewed papers will be contacted in case of any missing details about their studies.

Data synthesis

A meta‐analysis of outcomes combining various studies included in the review shall be done. We will assess statistical heterogeneity with I 2 , which will indicate the percentage of the total variation across studies: 0%–40% low heterogeneity, 30%–60% moderate heterogeneity, 50%–90% may represent substantial heterogeneity and 75%–100% is considerable heterogeneity. If there is a substantial amount of heterogeneity (75%), then sources of heterogeneity will be examined through subgroup and sensitivity analyses. We will also use χ 2 test to test the heterogeneity and consider p<0.05 as statistically significant. A fixed‐effects model will be selected for significant homogeneous studies; otherwise we will apply a random‐effects model. All outcomes will be summarised using ORs and 95% CI. An OR <1 will represent a lower rate of outcome among the group of patients who were treated following the guidelines. Publication bias will be assessed by visual inspections of funnel plots and Egger’s test.

We will also provide a narrative synthesis of the findings from the included studies. The narrative synthesis shall be structured by describing the studies according to the type of intervention used. This will include the three categories of interventions recommend in the PUPPG guideline 9 :

Prevention of PUs, including risk factors and risk assessment, skin and tissue assessment, preventive skin care and emerging therapies for prevention of PUs.

Interventions for prevention and treatment of PUs, such as nutrition in PU prevention and treatment, repositioning and early mobilisation, repositioning to prevent and treat PUs, support surface and medical device-related PUs.

Treatment of PUs, for example, assessment of PUs and monitoring of healing, pain assessment and treatment, wound care, assessment and treatment of infection and biofilms, wound dressings for treatment of PUs and surgery for PUs. Results will be presented in tables, figures and graphs, followed by discussion.

Publication bias will be assessed in all analyses synthesising 10 or more studies to ensure adequate power in the analysis. 18 For investigation of the effect of small studies and publication bias, data from included studies will be entered into a funnel plot asymmetry test if we have at least 10 studies in the meta-analysis. Egger’s statistical test will be implemented using STATA/SE V.13 (StataCorp). The quality of supporting evidence will be assessed by the Grades of Recommendation, Assessment, Development and Evaluation. 19

Patient and public involvement

No patient involved.

Ethics and dissemination

This review will only use published literature and will not recruit participants. Therefore, no formal ethical approval or consent is necessary. It is anticipated that this systematic review will provide a detailed summary of the evidence of the effectiveness of the PUPPG in preventing the occurrence of PUs among elderly patients in hospital. It is also expected that the study will provide recommendations on the best PU preventive strategies applicable in healthcare settings. We aim to publish the research findings in a peer-reviewed scientific journal to promote knowledge transfer, as well as in various media, such as: conferences, seminars, congresses or symposia in a traditional manner.

Acknowledgments

The authors would like to thank Lindsey Sikora (librarian) for counselling in developing the searching strategies.

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Supplementary materials

Supplementary data.

This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

• Data supplement 1

AWB and HM are joint first authors.

AWB and HM contributed equally.

Contributors AWB, HM and WC contributed to the conception of the research question and writing of the protocol. HM, AWB, WC, MDFM and DAF contributed to the development of search strategies, eligibility criteria and methodology for data synthesis. HM, AWB, WC, MDFM and DAF contributed to drafting of the protocol and provided approval for the final version of this protocol. HM, AWB and WC will work in duplicate to screen the titles and abstracts of all the materials obtained using the search strategy to exclude the articles that do not meet the eligibility criteria. HM, AWB and WC will evaluate the potentially eligible studies with the full text and further exclude studies with documentation of the reason for exclusion. All authors will contribute to the bias assessment strategy and data extraction criteria. HM, AWB and WC will independently extract data from the included studies. HM, AWB and WC will analyse the data and draft the manuscript. All authors will read, provide feedback and approve the final manuscript.

Funding This work was supported by Hunan Provincial Key Laboratory of Nursing, grant number (2017TP1004), Hunan Provincial Science and Technology Department, China.

Competing interests None declared.

Patient consent for publication Not required.

Provenance and peer review Not commissioned; externally peer reviewed.

Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

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Effectiveness on hospital-acquired pressure ulcers prevention: a systematic review

Affiliations.

• 1 Faculty of Human Kinetics, Aventura Social, University of Lisbon, Lisbon, Portugal.
• 2 Faculty of Medicine, Environmental Health Institute (ISAMB), University of Lisbon, Lisbon, Portugal.
• 3 Faculty of Human Kinetics, Interdisciplinary Center for the Study of Human Performance (CIPER), University of Lisbon, Lisbon, Portugal.
• 4 School of Nursing and Midwifery, Royal College of Surgeons in Ireland, Dublin, Ireland.
• PMID: 31264345
• PMCID: PMC7948629
• DOI: 10.1111/iwj.13147

The effective approach on pressure ulcer (PU) prevention regarding patient safety in the hospital context was evaluated. Studies were identified from searches in EBSCO host, PubMed, and WebofScience databases from 2009 up to December 2018. Studies were selected if they were published in English, French, Portuguese, or Spanish; incidence of PUs was the primary outcome; participants were adults (≥18 years) admitted in hospital wards and/or units. The review included 26 studies. Studies related to prophylactic dressings applied in the sacrum, trochanters, and/or heels, education for health care professionals, and preventive skin care and system reminders on-screen inpatient care plan were effective in decreasing PUs. Most of the studies related to multiple intervention programmes were effective in decreasing PU occurrence. Single interventions, namely support surfaces and repositioning, were not always effective in preventing PUs. Repositioning only was effective when supported by technological pressure-mapping feedback or by a patient positioning system. Risk-assessment tools are not effective in preventing PUs. PUs in the hospital context are still a worldwide issue related to patient safety. Multiple intervention programmes were more effective in decreasing PU occurrence than single interventions in isolation. Single interventions (prophylactic dressings, support surfaces, repositioning, preventive skin care, system reminders, and education for health care professionals) were effective in decreasing PUs, which was always in compliance with other preventive measures. These results provide an overview of effective approaches that should be considered when establishing evidence-based guidelines to hospital health care professionals and administrators for clinical practice effective in preventing PUs.

Keywords: effectiveness; hospital-acquired pressure ulcers; patient safety; pressure injury; prevention.

© 2019 Medicalhelplines.com Inc and John Wiley & Sons Ltd.

Publication types

• Meta-Analysis
• Systematic Review
• Administration, Topical
• Case-Control Studies
• Dermatologic Agents / therapeutic use
• Follow-Up Studies
• Hospitalization / statistics & numerical data*
• Inpatients / statistics & numerical data
• Patient Positioning
• Practice Guidelines as Topic*
• Pressure Ulcer / prevention & control*
• Primary Prevention / methods*
• Randomized Controlled Trials as Topic
• Severity of Illness Index
• Skin Care / methods*
• Time Factors
• Wound Healing / physiology
• Dermatologic Agents

Grants and funding

• SFRH/BD/122219/2016/Fundação para a Ciência e a Tecnologia
• BD609/2016/Universidade de Lisboa

• Research article
• Open access
• Published: 16 May 2015

Knowledge and practice of nurses towards prevention of pressure ulcer and associated factors in Gondar University Hospital, Northwest Ethiopia

• Nurhusien Nuru 1 ,
• Fisseha Zewdu 2 ,
• Senafikish Amsalu 3 &
• Yohannes Mehretie 4  

BMC Nursing volume  14 , Article number:  34 ( 2015 ) Cite this article

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Pressure ulcers are the common conditions among patients hospitalized in acute and chronic care facilities and impose significant burden on patients, their relatives and caregivers. Pressure ulcers have been described as one of the most costly and physically debilitating complications since the 20 th century. The pain and discomfort due to pressure ulcer prolongs illness, rehabilitation, time of discharge and even contribute to disability and death. This study was aimed to assess knowledge, practice and factors associated with pressure ulcer prevention among nurses in Gondar University Hospital, North-west Ethiopia.

An institution-based cross-sectional survey was conducted from March 15 - April 10, 2014 among 248 nurses in Gondar University hospital. A pretested and structured self-administered questionnaire was used for data collection. Data were entered using EPI info version 3.5.3 statistical software and analyzed using SPSS version 20 statistical package. Descriptive statistics was used to describe the study population in relation to relevant variables. Bivariate and multivariate logistic regression was also carried out to see the effect of each independent variable on the dependent variable.

Nearly half (54.4 %) of the nurses had good knowledge; similarly 48.4 % of them had good practice on prevention of pressure ulcer. Educational status [Adjusted Odds Ratio (AOR) = 2.4, 95 % CI (1.39-4.15)], work experience [AOR = 4.8, 95 % CI (1.31-10.62)] and having formal training [AOR = 4.1, 95 % CI (1.29-9.92)] were significantly associated with knowledge on prevention of pressure ulcer. While, satisfaction with nursing leadership [AOR = 1.9, 95 % CI (1.04-3.82)], staff shortage [AOR = 0.07, 95 % CI (0.03-0.13)] and inadequate facilities and equipment [AOR = 0.4, 95 % CI (0.19-0.83)] were found to be significantly associated with the practice on prevention of pressure ulcer.

Knowledge and practice of the nurses regarding prevention of pressure ulcer was found to be inadequate. Having higher educational status, attending formal training and being experienced were positively associated with knowledge; while shortage of facilities and equipments, dissatisfaction with nursing leadership and inadequate staff number showed negative association with practice of nurse’s pressure ulcer prevention. In-service training and upgrading courses are some of the important steps to improve nurses’ knowledge and practice on prevention of ulcer pressure.

Peer Review reports

Pressure ulcers are the common conditions among patients hospitalized in acute and chronic care facilities and impose a significant burden on patients, their relatives and caregivers [ 1 ]. Now days, pressure ulcers are recognized worldwide as one of the five most common causes of harm to patients and preventable patient safety problem. Also increasingly described as an indicator of the quality of care provided by health care organizations [ 2 - 4 ].

Pressure ulcers have been described as one of the most costly and physically debilitating complications since the 20 th century. The pain and discomfort of pressure ulcer delays rehabilitation, prolongs illness and timing of discharge, and also contribute to disability and death. These dramatically raise health care costs as a result of the need for supplies and nursing hours [ 5 ]. Moreover, health care budgets expend billion of dollars worldwide on prevention and treatment of patients with extended hospital stays from pressure ulcer development [ 6 ]. It has been estimated that the cost of treating pressure ulcer is 2.5 times higher than the cost of preventing [ 7 ]. In USA, pressure ulcers remain a major health problem affecting approximately 3 million adults [ 8 ]. A systematic review of 31 studies found that pressure ulcers significantly limit many aspects of an individual’s well-being, including general health and physical, social, financial and psychological quality of life [ 9 ]. So, the burden of pressure ulcers goes beyond increasing health care costs to loss of life [ 10 ].

According to an international literature, it has been identified that nurses’ knowledge of the prevention of pressure ulcers is poor, which is reflected in their practices as they do not comply with best practice guidelines [ 11 ]. Study conducted in Sweden on nurses’ knowledge and practice of existing guidelines on prevention of pressure ulcer found that, majority of them had inadequate knowledge and practice to implement guidelines [ 12 ]. Similarly, a study in Belgian Hospital found that knowledge of nurses about the prevention of pressure ulcers was inadequate [ 13 ]. Poor knowledge and practice of nurses have its own significant contribution for higher prevalence of pressure ulcers [ 14 ]. Moreover, a study in Bahir Dar, Ethiopia found that a total of 71 pressure ulcers were detected in 422 patients, with the prevalence rate of 16.8 %. The prevalence of pressure ulcer was higher in male respondents than in female respondents [ 15 ].Because, even if the prevention of pressure ulcers is a multidisciplinary responsibility, usually nurses play a major role and it is considered to be an essential part of nursing care in high income countries. Thus preventing ulcer should be the goal of all nurses [ 16 ] but it is rarely researched in low income countries like Ethiopia.

In Ethiopia there is lack of evidence on nurses’ knowledge and practice of pressure ulcer prevention. Therefore, this study set out to assess the level of nurses’ knowledge and practice on prevention of pressure ulcer and thereby generate appropriate information that can be used by program managers and stakeholders in the prevention and interventions of pressure ulcer.

Study design and set up

An institutional based cross sectional study was conducted among nurses working in Gondar University hospital. The hospital is located in Gondar town, Amhara regional state Northwest Ethiopia. Gondar is 740 km from the capital Addis Ababa. The hospital was established in 1954 and provides outpatient and inpatient services for more than 5 million peoples living in its catchment area.

Sample size and sampling procedure

The sample size was determined by using single population proportion formula with the assumption of: 50 % proportion, 95 % confidence level and 5 % margin of error. Given that the source population was less than 10,000 correction formula was used and 5 % non-response was added, making the final sample size 201. Since the total number of nurses working in the hospital was 255, the study involved all of them to increase the power of the study.

Data collection tool and procedure

Data were collected using a structured and pretested self administered questionnaire. The questionnaire and the consent form were prepared in English. Participants were asked 22 knowledge based and 22 practice based questions to assess their level of knowledge and practice towards prevention of pressure ulcer. Four midwife nurses and Public Health Officers collected the data with close supervision. Data quality was controlled by giving trainings and appropriate supervisions for data collectors. The overall supervision was carried out by the principal investigator. A pre-test was conducted using 6 % of the questionnaire on nurses who were working in Bahir Dar Referral Hospital. Appropriate modifications were made after analyzing the pretest result before the actual data collection.

The appropriateness of the instrument was measured through a pre-testing exercise, and the constraining factors were rectified. Prior to applying the survey instrument, the researchers engaged different expert reviewers as subject matter specialists at Gondar University Hospital to evaluate and finalize the instrument. Regarding to the reliability, the study used Cronbach’s coefficient alpha to measure consistency, complementarily and correlation coefficient. To generate the Cronbach’s alpha results, validation of the instrument was conducted through a pilot study and the results obtained had an overall Cronbach’s alpha of (r) = 0.76.

Operational definitions

• Pressure ulcer

a lesion of skin or underlying tissues by direct unrelieved pressure for more than 3 hours on the skin.

Good knowledge

Nurses, who scored above the mean score of the knowledge questions, were considered as having good knowledge on pressure ulcer prevention. But in the contrarily, those scored below the mean value considered as having poor knowledge towards prevention of pressure ulcer.

Good practice

Nurses who scored above the mean score of the practice questions related to prevention of pressure ulcer were considered to have good practice. But in the contrarily, those who scored below the mean score were considered as having poor practice towards prevention of pressure ulcer.

Data processing and analysis

The questionnaires filled by the nurses were checked for completeness and entered into EPI INFO version 3.5.3 statistical software and then exported to SPSS version 20 for further analysis. Descriptive statistics was used to describe the study population in relation to relevant variables. Both bivariate and multivariate logistic regression models were used to identify associated factors. Odds Ratios and their 95 % Confidence Intervals were computed and variables with p - value less than 0.05 were considered as significantly associated with the outcome variable.

Ethical considerations

Ethical clearance was obtained from University of Gondar, Ethical Review Committee of Department of Nursing. A formal letter of cooperation was written to Gondar University Hospital. After the purpose and objective of the study had informed, verbal consent was obtained from each study participant. Data were kept anonymously in the distributed questionnaire in order to keep confidentiality.

Socio-demographic characteristics of the study participants

Out of the expected 255 respondents, 248 agreed to participate in the study, yielding a response rate of 97.3 %. The mean age of the respondents was 28.25 years (SD = 5.1). Around half (53.6 %) were single. Nearly half of them (50.8 %) were males, two third (62.5 %) of the nurses had bachelor degree. Most (92.7 %) had working experience of less than 10 years (Table  1 ).

Organizational factors on prevention of pressure ulcer

Majority (91.1 %) of the nurses had not received any formal training and 223 (89.9 %) of them were not using any existing guidelines about risk assessment and prevention of pressure ulcer. More than half of the nurses (53.2 %) were not satisfied with the nursing leadership of the hospital. More than three quarter (78.6 %) of the nurses disagreed to the time given for each patient care. While Less than half (43.5 %) of the nurses reported staff shortage, big majority (88.3 %) of them agreed the hospital had inadequate facilities and equipments (Table  2 ).

Knowledge of pressure ulcer prevention

Participants were asked 22 questions to assess their knowledge on pressure ulcer prevention, and they were categorized in to two groups based on their score in relation to the mean. The mean score was 12.79 (SD = 3.21). More than half (54.4 %) of the respondents were found to have good knowledge, while a substantial proportion (45.6 %) of the respondents were not (Fig.  1 ).

Nurses’ knowledge and practice regarding to prevention of pressure ulcer, Gondar University Hospital, Northwest Ethiopia, 2014

From the six dimensions of knowledge regarding prevention of pressure ulcer, the nurses had a poor knowledge on three including risk assessment, skin care and management for mechanical loads. But, they possessed a good knowledge on factors related to pressure ulcer formation (M = 71.9, SD = 25.2), benefit of nutrition to maintain healthy skin (M = 69.9, SD = 29.1) and importance of staff training (M = 60.7, SD = 34.2) (Table  3 ).

Nurses’ practice regarding to prevention of pressure ulcer

By using 22 practice based questions, the mean practice score of the respondents was found to be 12.16 (SD = 9.75) (Table  4 ). Nearly half (48.4 %) of the respondents had good practice; whereas the remaining 51.6 % respondents had poor practice of pressure ulcer prevention (Fig.  1 ).

Factors associated with nurses’ knowledge regarding to prevention of pressure ulcer

Level of education, length of work experience and formal training on prevention of pressure ulcer were found to have significant and independent effect on nurses’ knowledge regarding to prevention of pressure ulcer, while availability of guidelines about pressure ulcer prevention was not significantly associated at p-value of < = 0.05.

Those nurses who had bachelor degree were 2.4 times [AOR = 2.4, 95 % CI (1.39-4.15)] more likely to have a good knowledge on prevention of pressure ulcer as compared to those nurses who had diploma. Nurses who had work experience of 11-20 years were 4.8 times [AOR = 4.8, 95 % CI (1.31-10.62)] more likely to have good knowledge than nurses with less than 10 years of work experience.

Those nurses who had formal training about pressure ulcer were 4.1 times [AOR = 4.1, 95 % CI (1.29-9.92)] more likely to have good knowledge than those nurses who did not took training about pressure ulcer (Table  5 ).

Factors associated with nurses’ practice of pressure ulcer prevention

Satisfaction with nursing leadership, Having formal training on pressure ulcer prevention, staff shortage and inadequate facilities and equipments were found to have significant and independent effect on practice of nurses’ towards prevention of pressure ulcer, while level of education, length of work experience were not significantly associated at p-value of < = 0.05.

Nurses who were satisfied with nursing leadership were around 2 times [AOR = 1.9, 95 % CI (1.04-3.82)] more likely to have good practice of pressure ulcer prevention when compared to those who were not. Study participants who agreed about staff shortage in the work place were 93 % [AOR = 0.07, 95 % CI (0.03-0.13)] less likely to have good practice than nurses who disagreed about the shortage of staff. Moreover, respondents who agreed about inadequate facilities and equipments in the work place were 60 % [AOR = 0.4, 95 % CI (0.19-0.83)] less likely to have good practice towards prevention of pressure ulcer as compared to those who were disagree about inadequate facilities and equipments (Table  6 ).

Prevention of pressure ulcers is an indicator of quality of care. Nursing care has a major effect on pressure ulcer development and prevention. Hence, Pressure ulcers are a major nurse-sensitive outcome [ 16 ]. So this study was aimed to describe the level of nurse’s knowledge and practice on prevention of pressure ulcers and its associated factors in Gondar University Hospital, Northwest Ethiopia.

In this study, 54.4 % of the participants were found to be knowledgeable. While substantial proportions 45.6 % were not, this is inadequate. Because, as they are nurses working in recognized teaching referral hospital, and are expected to be well experienced, this level of knowledge is below the anticipated. The finding of this study is comparable with other studies conducted in different parts of the world. In a study conducted in Turkey the mean score of correct answer was 48.85 % [ 17 ] and the study conducted in Belgian hospital revealed that the mean knowledge score was 49.7 % [ 13 ]. Similarly, the study conducted in Bangladesh indicated that the overall nurses’ knowledge on pressure ulcer prevention were found to be 57.79 % [ 18 ] and the other study conducted in one of the largest health insurance hospital in Alexandria, found that, the overall mean percentage score for nurses were below the minimum acceptable level [ 19 ].

Respondent’s formal education and training experience may be a factor related to this poor level of knowledge. Pressure ulcer prevention related content included in their curriculums might not be sufficient. In addition, lack of learning resources for nurses to update their knowledge would be another reason for the poor level of knowledge. Specifically in Ethiopia, there is a limited learning resource for nurses to update their knowledge. Moreover nursing journals are not available even at the nursing institutes or hospitals. Specific to this study 91.1 % of the participants had not received any formal training and 89.9 % of the nurses were not using any existing guidelines on risk assessment and prevention of pressure ulcer.

Respondent’s level of education was found to be significantly associated with knowledge of pressure ulcer prevention. This finding is in line with the study conducted in Sweden among registered nurses and licensed practicum nurses in which the registered nurses’ score were significantly higher than those of the licensed practicum nurses [ 20 ]. This could be attributed to the possibility that more educated respondents have a higher opportunity of exposure to different courses directly or indirectly related to prevention of pressure ulcer.

Respondents with work experience of 11-20 years had good knowledge when compared to those with work experience of ≤ 10 years. Similar finding was reported in study conducted in Nigeria; where years of experience were significantly associated with clinical practice and knowledge [ 21 ]. Other study done in Spain on Nurses’ knowledge and clinical practice of pressure ulcer care revealed that, the greater the working experience the higher the knowledge gained [ 22 ]. The reason might be nurses with more years of working experience have more chance to work with different professionals so that they can learn from their coworker’s experience. Also since they have more prolonged exposure to patient care, they have greater chance to learn how to prevent pressure ulcer even from their own mistakes as compared to those who have less years of working experience.

Nurses who took formal training on pressure ulcer prevention were found to have good knowledge than those who had not. Similarly in a study conducted in Swedish healthcare to assess knowledge, attitude and practice of nursing staff on pressure ulcer prevention; nurses who had training were more knowledgeable than those who did not [ 23 ]. This might be due to the fact that training increases the chance of the trainees to get up to date information about pressure ulcer related preventions.

Staff shortage is one of the factors associated to nurse’s practice in prevention of pressure ulcer. This study also favored the above claim in which, respondent’s practice of pressure ulcer prevention was found to be poor which was less than 50 %. Similarly study conducted in England showed that, majority of the nurses reported lack of staff and time as barrier to implement effective care practices related to prevention of pressure ulcer [ 24 ]. The poor practice can be explained by the fact that, shortage of nursing staff limits the working time available for each patient’s care. Especially in countries like Ethiopia where number of health professionals is near to the ground, inadequate nurse to patient ratio may limit the implementation of quality care related to pressure ulcer prevention.

In this study more than three fourth of nurses did not use a risk assessment scale. Similarly the study conducted in Sydney found that 79 % of the nurses did not use any assessment tool to identify patients with at risk of pressure ulcer [ 25 ]. This can be explained by lack of evidence based nursing practice and in-service training on prevention of pressure ulcer.

Respondents who were satisfied with the nursing leadership had good practice as compared to those who were not. Possible reason for this result might be nurses who are satisfied with the nursing leadership are happier on their working environment, so that they are motivated to invest all their knowledge and experiences on practices related to prevention of pressure ulcer.

Inadequate facilities and equipments in the workplace were associated with poor practice on prevention of pressure ulcer. This might be due to the fact that limited access to adequate facilities and equipments may hinder nurse’s motivation and ability to prevent patients from developing pressure ulcer.

Using a self reported questionnaire to examine the nurses’ practice towards prevention of pressure ulcer was the main limitation of this study.

Conclusions

Nurses’ knowledge and practice regarding prevention of pressure ulcer was found to be inadequate. Having higher educational status, attending formal training, being more experienced showed a positive and significant association with knowledge; whereas inadequate facilities and equipments, dissatisfaction with the nursing leadership and staff shortage and were found to be associated with poor practice of pressure ulcer prevention. In-service training, upgrading courses and ensuring availability of the necessary facilities and equipments are some of the important steps to improve nurses’ knowledge and practice regarding to prevention of pressure ulcer.

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Acknowledgements

Our heartfelt thank goes to University of Gondar for all expenses of the research work and all the study participants who voluntarily participated in this study.

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Nurhusien Nuru

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Fisseha Zewdu

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NNY, FZA and SAF were involved in the design of the study, data analysis, and interpretation of the findings, report writing and manuscript preparation. YMA was involved in the design of the study, analysis and interpretation of the data, and review of the report. All authors read and approved the final manuscript.

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Nuru, N., Zewdu, F., Amsalu, S. et al. Knowledge and practice of nurses towards prevention of pressure ulcer and associated factors in Gondar University Hospital, Northwest Ethiopia. BMC Nurs 14 , 34 (2015). https://doi.org/10.1186/s12912-015-0076-8

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18 April 2024

Smith+nephew announces new evidence supporting allevyn◊ life foam dressing’s role in pressure injury prevention.

Smith+Nephew (NYSE:SNN; LSE:SN), the global medical technology company is pleased to announce exciting data for its ALLEVYN LIFE Dressing in a recent study by Professor Amit Gefen and his research group published in the International Wound Journal, 1 that shows a novel mechanism of action relating to pressure injury prevention (PIP).

The study found that due to the independent and non-bonded internal layers of ALLEVYN LIFE Dressing, a layer-on-layer sliding phenomenon occurs and allows for dissipation of mechanical energy that could otherwise be transferred to the patient in a bonded dressing. 1

The results show that layer-on-layer frictional sliding of ALLEVYN LIFE Dressing absorbs 30-45% of the mechanical energy, which could help alleviate pressure injury incidence in a patient's skin and underlying soft tissues. This novel mechanism of action further adds to our understanding of how multi-layer dressings such as ALLEVYN LIFE work when used prophylactically for PIP. 1

“Based on my extensive, decades-long research in pressure ulcer/injury prevention, I am certain that an effective prevention dressing must contain a shear mitigation mechanism,” said Amit Gefen, Professor of Biomedical Engineering at Tel Aviv University. “My recent study published in the International Wound Journal on ALLEVYN LIFE Dressing revealed the role of its unique internal frictional layer-on-layer sliding which, together with its specific construct and material composition, facilitate effective shear mitigation.”

“Pressure injuries have a high burden on patients and healthcare systems,” said Rohit Kashyap, President, Advanced Wound Management at Smith+Nephew. “This alignment of the laboratory findings with the clinical literature clearly demonstrates the enhanced clinical efficacy of ALLEVYN LIFE Dressings in helping reduce the burden of preventable pressure injuries as one of the only 5-layer foam dressings with independent, non-bonded layers.”

Pressure injuries remain one of the most significant healthcare challenges globally that affects patients of all ages. 1 On average, a pressure injury leads to increased healthcare costs of $21,767 per patient and an extra 9.5 days in hospital. 8

The study introduced a novel method to thoroughly test the frictional sliding capabilities of the independent layers of ALLEVYN LIFE Dressing. A new metric, frictional energy absorber effectiveness (FEAE), was also introduced to quantify the total mechanical energy dissipation of ALLEVYN LIFE Dressing. 1

This newly discovered mechanism of action for ALLEVYN LIFE Dressing further adds, and gives context to, the already existing wealth of clinical evidence9 for its capabilities in PIP that demonstrate significant reduction in pressure injury incidence. *1

To read the full publication please click here . To learn more about ALLEVYN LIFE Foam Dressings please click here .

About Smith+Nephew

Smith+Nephew is a portfolio medical technology business that exists to restore people’s bodies and their self-belief by using technology to take the limits off living. We call this purpose ‘Life Unlimited’. Our 19,000 employees deliver this mission every day, making a difference to patients’ lives through the excellence of our product portfolio, and the invention and application of new technologies across our three global business units of Orthopaedics, Advanced Wound Management and Sports Medicine & ENT.

Founded in Hull, UK, in 1856, we now operate in more than 100 countries, and generated annual sales of $5.2 billion in 2022. Smith+Nephew is a constituent of the FTSE100 (LSE:SN, NYSE:SNN). The terms ‘Group’ and ‘Smith+Nephew’ are used to refer to Smith & Nephew plc and its consolidated subsidiaries, unless the context requires otherwise.

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• Marché C, Creehan S, Gefen A. The frictional energy absorber effectiveness and its impact on the pressure ulcer prevention performance of multilayer dressings. Int Wound J. 2024; 21(4):e14871.
• Smith+Nephew 2016. Permeability of Hydrophillic Polyurethane Film when in contact with water and water vapour (ALLEVYN LIFE). Internal Report. RD/16/019.
• Tiscar-González V, Menor-Rodríguez MJ, Rabadán-Sainz C, et al. Clinical and Economic Impact of Wound Care Using a Polyurethane Foam Multilayer Dressing. Adv Skin Wound Care. 2021;34(1):23–30.
• Smith+Nephew 2016. Wound Model Testing of New ALLEVYN Life Gen2 wcl Dressing using Horse Serum at a Flow Rate Modelling that of a Moderately Exuding Wound. DS/14/303/R
• Rossington A, Drysdale K, Winter R. Clinical performance and positive impact on patient wellbeing of ALLEVYN Life. Wounds UK. 2013;9(4):91–95
• Clarke R. Positive patient outcomes: The use of a new silicone adhesive foam dressing for pressure ulcer prevention and treatment. Paper presented at: CAET; 2013
• Lisco C. Evaluation of a new silicone gel-adhesive hydrocellular foam dressing as part of a pressure ulcer prevention plan for ICU patients. Paper presented at: WOCN; 2013
• Wassel C, Delhougne G, Gayle J, et al. Risk of readmissions, mortality, and hospital-acquired conditions across hospital-acquired pressure injury (HAPI) stages in a US National Hospital discharge database. Int Wound J. 2020; 1–11.
• Smith+Nephew 2021. ALLEVYN Dressing’s PIP evidence compendium. 31817. Available at: https://smith-nephew.stylelabs.cloud/api/public/content/allevyn-dressings-pip-compendium-2021?v=f6cfe376

• Open access
• Published: 20 April 2024

Developing an interprofessional decision support tool for diabetic foot ulcers management in primary care within the family medicine group model: a Delphi study in Canada

• Magali Brousseau-Foley 1 , 2 ,
• Virginie Blanchette 1 , 3 ,
• Julie Houle 4 &
• François Trudeau 1  

BMC Primary Care volume  25 , Article number:  123 ( 2024 ) Cite this article

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Metrics details

Primary care professionals encounter difficulties coordinating the continuum of care between primary care providers and second-line specialists and adhere to practice guidelines pertaining to diabetic foot ulcers management. Family medicine groups are providing primary care services aimed to improve access, interdisciplinary care, coordination and quality of health services, and reduce emergency department visits. Most professionals working in family medicine groups are primary care physicians and registered nurses. The aim of this study was to develop and validate an interprofessional decision support tool to guide the management of diabetic foot ulcers for primary care professionals working within the family medicine group model.

A one-page decision tool developed by the research team was validated by an expert panel using a three-round Delphi protocol held between December 2019 and August 2021. The tool includes 43 individual actions and a care pathway from initial presentation to secondary prevention. Data collection was realized with both paper and electronic questionnaires, and answers were compiled in an electronic spreadsheet. Data was analyzed with use of descriptive statistics, and consensus for each item was defined as ≥ 80% agreement.

Experts from 12 pre-identified professions of the diabetic foot ulcer interdisciplinary care team were included, 39 participants out of the 59 invited to first round (66.1%), 34 out of 39 for second (87.2%) and 22 out of 34 for third (64.7%) rounds. All items included in the final version of the decision support tool reached consensus and were deemed clear, relevant and feasible. One or more professionals were identified to be responsible for every action to be taken.

Conclusions

This study provided a comprehensive decision support tool to guide primary care professionals in the management of diabetic foot ulcers. Implementation and evaluation in the clinical setting will need to be undertaken in the future.

Peer Review reports

Introduction

Diabetes mellitus prevalence has been constantly on the rise for over two decades. Worldwide, 536.6 million people were living with diabetes in 2021 [ 1 ]. In Canada, this represents 10% of the population in 2022 [ 2 ]. Lifetime risk of suffering from a diabetes-related foot ulcer (DFU) is estimated at 34%, with a 20% risk of limb amputation [ 3 ]. A DFU is defined as “a foot ulcer in a person with current or previously diagnosed diabetes mellitus, and usually accompanied by peripheral neuropathy and/or peripheral artery disease in the lower extremity” [ 4 ]. Adherence to a comprehensive evidence-based coordinated treatment regimen provided by an interdisciplinary care team decreases the need for major amputations and improves healing rates [ 3 , 5 , 6 ]. However, current clinical practices in primary care, specifically within the family medicine group (FMG) model in the province of Quebec, Canada, have difficulties to adhere to DFUs management guidelines, plus coordinating the continuum of care between primary care professionals and second-line specialists. An audit previously conducted by our research team highlighted some issues that led people with diabetes to be admitted to our regional hospital because of a DFU or a DFU complication as the main admission diagnosis [ 7 ]. The following discrepancies from current best practice recommendations were identified: absence of a DFU team resulting in poor coordination of care, silo work from health professionals, inefficient communication between stakeholders, lack of knowledge about the scope of practice of other professions relevant to DFU care, insufficient wound care training and inability to prioritize concurrent health needs in this complex population. Therefore, there is a failure to provide their patients with the best possible chance for healing DFUs and avoiding amputations [ 8 , 9 , 10 ]. FMGs provide most of the primary care services to Quebec’s population since their establishment in 2002 as a means to improve access, interdisciplinary care, coordination and quality of health services, and reduce emergency department visits [ 11 , 12 ]. FMGs professionals are mostly primary care physicians (PCPs) supported by registered nurses (RN) usually in a 4 to 6 PCPs to 1 RN ratio based on number of people enrolled in the FMG. It encourages PCPs to be available in priority, if not exclusively, to people enrolled in his or her FMG. The model was developed so RN could alleviate PCPs workload by taking care of minor ailments not requiring physician expertise [ 13 ]. Other healthcare professionals (physiotherapists, psychologist, social workers, etc.) are also sometimes present. Moreover, in exchange for its staff and material resources being partially financed by the public health system, the FMG has the obligation to offer medical services in the evenings and weekends. The FMG model was therefore mostly developed to provide increased access and continuity of care in the mean of extended practice hours and added professionals, rather than true interdisciplinary care, which is more dependent on each clinic local organization and available staff [ 14 ]. Despite its specificities, the FMG model in Quebec, Canada, can been seen as a variation of other team-based primary care models elsewhere in the world where professionals offer longitudinal continuous general healthcare services [ 12 ]. In the absence of dedicated wound clinics, DFU assessment and management often falls under the responsibility of FMGs professionals, whom then frequently refer patients to state-financed healthcare community services or podiatric private practices when patients have private insurances covering these services.

The need for a decision support tool to guide DFUs’ management has already been expressed in various clinical settings [ 15 , 16 , 17 , 18 ] but was never addressed specifically for the Quebec’s FMG model, where only a few clinical settings have access to specialized wounds clinics [ 8 , 19 , 20 ]. Practice guidelines originating from national [ 21 , 22 , 23 ] and international interest groups [ 6 , 24 ] are widely available but often represent documents not practical in clinical setting. Additionally, implementation of guidelines can be challenging as their recommendations can be heterogeneous [ 25 ]. Decision support tools developed for other complex medical problems managed in primary care proved to help with achieving better quality and more coherent care [ 26 , 27 ]. We therefore advocate that a decision support tool for DFU management in primary care could similarly improve outcomes in this population. A Delphi protocol was chosen as the most effective method to develop and validate the decision support tool. A Delphi protocol is an iterative, structured process, widely used in multiple disciplines, namely in health sciences, to obtain a consensus from answers to questionnaires based on anonymous opinions of a group of participants selected because of their personal expertise on a topic under study [ 28 ]. A Delphi protocol have previously been used to develop and validate decision aid tools for primary care professionals [ 29 , 30 ] and DFU management [ 31 , 32 ]. The purpose of this study is to develop and validate a comprehensive decision support tool to guide the management of DFUs diagnosed by professionals within FMGs. This validation process is necessary in order to ensure that the tool is relevant, clear and feasible before its implementation.

Decision support tool development

The interdisciplinary research team (MBF, VB, JH) and collaborators (a PCP, a RN and a podiatrist) developed a one-page decision tool to help FMGs’ professionals manage DFUs based on a rapid review of current literature including practice guidelines and related evidence-based literature [ 33 ] during the fall of 2019. Identified actions to be taken in the management of DFUs were classified according to the severity (uncomplicated vs complicated) and divided into professional roles to reflect what was available from the literature as well as professional practices in the province of Quebec.

Decision support tool validation

The initial version (43 items) of the decision support tool was validated through a modified Delphi protocol. This Delphi validation was led and reported according to the Guidance on Conducting and REporting DElphi Studies (CREDES) [ 34 ]. Because of the complexity of producing a structured, comprehensive and multidisciplinary tool, it was decided to diverge from the classical Delphi protocol which usually presents participants with open-ended questions in order to generate qualitative data that will become the items to be evaluated for consensus in subsequent rounds, hence the modified Delphi protocol [ 28 ]. The alternative pathways represented in the tool reflect well the adjustable composition of the ideal team [ 23 , 35 ]. Also, because of the facilitator’s role of filtering participants’ answers and providing controlled feedback, the final version of the tool cannot be totally exempt from the subjective interpretation of the authors on the matter [ 28 ]. A maximum number of three rounds to achieve consensus was predetermined in accordance with scientific evidence [ 28 ].

Figure  1 illustrates the modified Delphi protocol. Expert panel’s recommendations were collected for the first round from December 2019 to May 2020 using a three-part paper questionnaire and a one-page decision support tool in its initial version. Questionnaires developed by the research team for all three rounds are available in translated English language versions in Additional file 1 . The first part included 13 questions about participants sociodemographic and professional characteristics. The second part included 43 questions corresponding to each item of the decision support tool. For each item, the expert had to evaluate four criteria: the item is clear, relevant, feasible, and which healthcare professional should be responsible for it. The following definitions [ 36 ] were provided to guide participants:

Clarity means that the wording to describe the item is easily understandable;

Relevance indicates that the item is in relation to the matter at hand;

Feasibility means that one is capable of doing or of carrying out the action; and

Responsibility is liability for an action (based on the professional scope of practice, competencies and availability in the healthcare system organization).

Flow chart illustrating the stages of the modified Delphi protocol

The third part of the questionnaire asked three open-ended questions: 1) regarding additional items or supplementary resources that should have been included in the decision support tool, 2) if the graphic layout and organization of the tool was user-friendly and straightforward, and 3) if the participant had any additional comments. The time required to complete the first-round questionnaire was estimated at 60 to 90 min.

The second and third Delphi rounds were conducted through an online questionnaire using the Université du Québec à Trois-Rivières online questionnaire tool from March to May 2021 and from July to September 2021 respectively. The time required to complete questionnaires was approximately 15 min for the second round and approximately 5 min for the third round. The format was similar to the second part of the first-round questionnaire. A new section of the questionnaire allowed participants to determine which supplementary resources proposed in the first round should be included into the decision support tool. All experts from the first round were invited to participate. Items from the first round that reached consensus were removed. Controlled feedback regarding the previous round statistical aggregation of experts’ answers was provided both with an updated version of the decision support tool and through the questions developed from first-round items that did not meet consensus. The second-round questionnaire comprised a total of 34 questions.

For the third round of the Delphi questionnaire, all experts from the second round were invited to participate in the third round. Feedback regarding the previous round statistical aggregation of experts’ answers was provided both with an updated version of the decision support tool and through the questions developed from second-round items that did not meet consensus. The third-round questionnaire comprised a total of 4 questions.

Participants

As the projected decision support tool users are primary care professionals, an expert panel to validate its content and structure needed to include both content experts but also professionals with wound care management expertise representative of most professionals working in this environment. We aimed at inviting for the first round’s questionnaire five professionals from each 12 predetermined areas of expertise: 1) PCPs, 2) RNs, 3) podiatrists, 4) RNs specialized in wounds, 5) physiatrists, 6) occupational therapists, 7) physiotherapists, 8) orthotists, 9) infectious disease or internal medicine physicians, 10) vascular surgeons, 11) orthopedic surgeons, and 12) wound care researchers for a total of about 60 participants. An expert panel’s member had to individually and anonymously share their opinion in the questionnaires. All experts needed to have knowledge or clinical experience with the management of DFU in the province of Quebec, Canada. They had to be competent in French as this is the language in which the tool was developed, French being the official language of this province. Participants identified by the authors in their network of contacts were individually solicited to participate. All received an information letter and consent form to be signed. Delphi rounds took place between December 2019 and August 2021. The sample size was determined according to what is recommended for this study design [ 28 ] and based on the expected initial response rate and attrition rate throughout sequential Delphi rounds.

Ethics approval

This research project was performed in accordance with the declaration of Helsinki and received ethical approbation from the Centre intégré universitaire de santé et de services sociaux de la Mauricie-et-du-Centre-du-Québec ethical board CÉRM-2019–002. Written informed consent was obtained from all subjects.

Statistical analysis

All answers were entered into an Excel spreadsheet (Microsoft, version 16.16.7) for quantitative and qualitative analysis. Consensus threshold was defined as 80% agreement for each item. Clarity was noted as 0 (unclear) or 1 (clear). All items that did not reach 80% agreement for clarity were submitted with alternative wording in the next round. Relevance was evaluated with a four-point Likert scale (1 being of low relevance and 4 high relevance). For each item, values of three and four were considered as agreement. Feasibility was evaluated with a five-point Likert scale (1 being of low feasibility and 5 high feasibility). For each item, values four and five were considered as agreement. A relative frequency of 80% or higher of values three and four for an item was considered to have reached agreement consensus and was excluded from the next round. The choice between a four-point and a five-point Likert scale was based on the nature of the data to collect. Regarding relevance, because items were identified from evidence-based literature, a higher consensus was expected for the relevance criterion and it was chosen to avoid the possibility of a neutral response in order to force experts to take a stance. On the other hand, as resources are often limited within the healthcare system and vary in different geographical locations, neutral responses on a five-point scale was considered unfeasible and therefore excluded the item, as the tool had to propose actions achievable for most professionals no matter the care setting. For the responsibility criterion, participants had to choose from a predetermined list of professionals (PCP, RN, podiatrist, RN specialized in wound care, rehabilitation team, infectious disease specialist, vascular surgeon and orthopedic surgeon) or other and specify the professional title. The relative frequency in percentage of answers was calculated for each item. A choice of professional that reached a relative frequency of 20% and higher for an item was retained. It was therefore possible to have more than one professional identified as responsible for an item. In the absence of a clear consensus, all choices of professional individually and in all possible combinations were submitted in the second round. All open-ended answers were manually organized by subject and theme in the same spreadsheet. All additional resources to be added to the decision support tool suggested by participants more than three times in answer to open-ended questions were listed to be evaluated in the second round. In the second round, for each item and criterion, consensus threshold was calculated in the same manner as in the first round. Supplementary resources were evaluated using four-point Likert scales (1 being of low relevance and 4 high relevance of the proposed additional resource). Values of three and four were considered as agreement. A relative frequency of 80% or higher of values three and four for an item was considered to have reached agreement threshold. Supplementary resources that did not reach consensus were excluded. For the third Delphi round, a simple majority (50% and more agreement) was required to achieve consensus on each item and criterion.

Final version of decision aid tool

As the initial version of the decision aid tool was developed based on literature available in 2019, once data collection and analysis were completed, the research team verified if any significant changes appeared in national and international guidelines and best practice documents between 2019 and 2023 that would require to add to, remove or modify any items included in the tool. As for the additional resources to appear at the back of the tool selected by the expert panel, the hyperlinks and resources provided were chosen by the research team in 2023, prioritizing national resources when available and if not, resources from international organizations.

Delphi first round

Fifty-nine experts were invited to participate in the study. A total of 39 participants (66.1% response rate) returned the completed first-round questionnaire (mean age = 40.9 years old; SD = 10.21 years). All professional titles were represented by at least two participants except for occupational therapist which was not present. The first-round panel was composed mostly of PCPs and RNs (Table  1 ). A majority of experts were working in clinical settings (Table  2 ).

Participants were mostly women (64%). Participants accumulated 14.7 ± 9.2 (M ± SD) years of professional experience in their field and a mean of 8.3 ± 8.5 years specifically in wound care. Agreement obtained for all items and criteria for each Delphi round is detailed in Table  3 .

For responsibility, three items were shared between more than one professional, resulting in 13 possible individual professionals or combinations of professionals. Out of the 13 supplementary resources to be added to the decision support tool, nine reached consensus. The decision support tool was adjusted based on these results by the authors and graphic designer.

Delphi second round

Out of the 39 experts invited to the second round, a total of 34 participants (87.2% response rate) completed the second-round questionnaire. All professional titles were represented by at least two participants except for physiotherapist and occupational therapist. A majority of PCPs, RNs and RNs specialized in wounds made for 66.6% (26 participants) of the expert panel. Based on agreement, the decision support tool was again adjusted based on these results by the authors and graphic designer.

Delphi third round

Out of the 34 experts invited to the second round, a total of 22 participants (64.7% response rate) completed the third-round questionnaire. All professional titles were represented by at least one participant (infectious disease physician and orthotist) or more, except for physiotherapist, occupational therapist and orthopedic surgeon. A majority of PCPs, RNs and RNs specialized in wounds made for 63.6% (14 participants) of the expert panel. The decision support tool was adjusted for its final version based on the attained results, which was translated to English (Fig.  2 ). The complete final version of the tool in color and translated to English is available in Additional file 2 . The original French version in available in Additional file 3 .

Final version of the front page of the decision support tool (translated to English)

The front page of the tool is divided into three columns of different colors, from left to right green, orange and red, respectively representing actions to be taken for uncomplicated ulcers, wound care and complicated ulcers. The green column includes actions under the responsibility of primary care professionals (PCPs, RNs, and podiatrists if available). The orange column shows actions that may be realized by first or second-line professionals or by professionals working in community or private settings dependent on local care organizations. The red column lists actions and specifies reasons for referral to second-line specialists. Arrows indicate the direction of the pathway at different steps along the continuum of care, and symbols highlight important actions where primary care professionals might consider a referral to a second-line specialist. An updated rapid-review of the literature available in 2023 after data analysis was completed and did not compel any change in the items validated by the expert panel. The back of the tool provides up-to-date references and hyperlinks for additional resources to further inform and educate professionals to help them achieve evidence-based practices.

The purpose of this study was to develop and validate a comprehensive decision support tool to guide the assessment and management of DFUs in primary care. The tool was produced and validated using a Delphi protocol by an expert panel including professionals susceptible to compose an ideal interdisciplinary specialized wound care team. The tool targets primary care professionals in order to guide them in delivering coordinated care following up to date practice guidelines to people with DFU. It also serves to improve communications and trajectories between primary care professionals and second-line specialists. It is not intended to be used for screening and stratification of the at-risk diabetic foot in primary care as a recent validated tool is already available [ 37 ]. As any decision aid tool, it should not take precedent over health professionals’ clinical judgment.

It is demonstrated that timely and coordinated interventions for people with DFU with a specialized team involved in integrated prevention and care obtain better outcomes, namely improve DFU healing rates [ 35 ], reduce major amputations [ 38 , 39 ], and lower health care costs [ 40 , 41 ]. However, DFU specialized teams are not available and integrated care is absent in the majority of Quebec and Canadian regions and there is heterogeneity in the resources available locally [ 42 ]. To our knowledge, this is the first study in Canada to develop and validate a decision support tool intended for FMG’s professionals, mostly PCPs and RNs, to be used as a care pathway and checklist of actions to be completed when taking care of people with a DFU. A recent study implemented an acute care DFU pathway for people requiring hospitalization, reducing length of stay and costs [ 18 ]. Yet, the interest of a tool to be used in primary care is to decrease the necessity for people with DFU to visit the emergency department and to be admitted to hospital. This is known to reduce costs [ 43 ] and morbidity [ 44 ] associated with hospital stays. We postulate that our tool could improve primary care professionals’ capacity to manage DFU and consequently could enhance outpatient care. This also aligns with the primary purpose that led to the development of FMGs, namely to provide continuity of care outside of the hospital setting [ 13 ]. FMGs’ teams usually know their enrollees well and are easily accessible, especially for those with chronic diseases such as diabetes. In that perspective, the patient’s primary care team is often best placed to coordinate the complex needs arising with the occurrence of a DFU. Unfortunately, many obstacles still exist in the healthcare system organization that sometimes makes it easier for professionals and patients to manage DFUs in a hospital setting.

The comments formulated by the expert panel members were not formally analyzed but were considered by the research team when adjusting the tool after each Delphi round. One main theme that was recurrent is the lack of equipment, poor access to the hospital technical platform and limited availability of professionals outside the FMG staff. This was especially true regarding the vascular evaluation that needs to be performed on initial presentation of a person with a DFU. Having access to simple equipment such as a portable Doppler with the proper probe was reported to be challenging for many experts. Even in a hospital setting, well-equipped vascular labs appeared to be as rare as dedicated interprofessional wound care teams. This explains why toe pressure or toe pressure index was not included in the tool. Also, long delays to obtain arterial Doppler or angiography through a radiology department was perceived to have a negative impact on DFU care quality. Current practice for most experts was therefore to consult with a vascular surgeon when vascular status was uncertain, and the tool was made to reflect this. Health promotion interventions such as nutritional evaluation and diabetic education were also identified as actions for which there were insufficient resources available, even though many experts highlighted the importance of patients’ empowerment and education to self-management of disease. In this instance, it was mostly due to time constraints rather than equipment or expertise as FMG professionals were deemed capable of providing this service, but the difficulty resided in time limitation secondary to an already excessive work load. Access to nutritionists and diabetes educators was also challenging for patients that depend solely on resources available through publicly funded healthcare. Similarly, lack of access to podiatrists, which is not covered by the public healthcare system in Quebec, was judged to have a negative impact on DFU management as they were considered by most experts to be the best professionals to provide wound debridement and decide on offloading modality. When a podiatrist was not implicated, many experts felt debridement and offloading were not done or were inadequately done. Finally, a very significant obstacle that was pointed out by numerous members of the expert panel is that most offloading modalities have to be paid out of pocket by patients, and for a large proportion, this financial burden is too much, transforming healable DFUs into maintenance wounds.

Access to limb preservation interventions prior to hospitalization is known to be heterogenous as shown in Ontario (Canada) and seems particularly inadequate in regions distant from major medical centers [ 45 ]. Providing PCPs with standardized criteria for referral to second line specialists before amputation becomes unavoidable could improve relevance and timing of consultations with vascular and orthopedic surgeons. It could also improve communication and facilitates collaboration between PCPs and tertiary center consultants through telemedicine when local resources are not available. Telemedicine has demonstrated benefits for the management of many complex diseases, including DFU [ 46 ]. Because the decision support tool is intended for primary care professionals, the same team of professionals that will continue to provide comprehensive healthcare after the DFU episode, their interventions might have a beneficial impact lowering DFU recurrence rate and improve limb preservation, as about 80% of amputations are preventable [ 47 ]. Such a tool as also the potential to serve as a basis to discuss basic prevention and health promotion interventions between health professionals and patients as it provides an overview of all that require consideration when caring for people with DFU. It might be of interest that future studies aim at transforming this tool into a knowledge transfer tool both for health professionals, their patients and caregivers.

It is needed to mention that the rapid-review that was conducted to develop the initial version of the decision aid tool submitted during the initial round of the Delphi validation was completed in 2019, and the three rounds of questionnaires took place from 2019 to 2021. However, no specific references were provided to the expert panel during the Delphi validation, only a list of items to be evaluated. Also, most items stated general recommendations regarding DFU evaluation and management which are unlikely to evolve with time so significantly as to become obsolete. Therefore, once data collection and analysis were completed, the research team verified if any changes appeared in national and international guidelines and best practice documents between 2019 and 2023 that would require to add to, remove or modify any items included in the tool. As there were no significant changes, the reference list was updated, and the tool remained the same. As for the additional resources provided at the back of the tool, the expert panel only provided a list of themes pertaining to DFU management rather than specific resources, therefore, the hyperlinks and resources selected were chosen by the research team once the Delphi process was completed, prioritizing national resources when available and if not, resources from international organizations. The English (Fig.  2 and Additional File 2 ) and French (Additional File 3 ) versions are different as in the original French version of the tool, French language resources were prioritized over English language resources when available and up to date.

Limitations

Some of the limitations inherent to the study design is the selection process of the expert panel, which could introduce a selection bias. However, we consider that our sample was representative in composition and proportions of both the main users (primary care professionals and second line specialists) and available resources within the local healthcare system organization. Even though only 25.64% of the first-round expert panel members currently worked within a FMG as their main occupation, many worked within a FMG as a secondary occupation or had worked in a FMG in the past. Moreover, 38.46% of experts were PCPs or RNs, the two mandatory professions composing FMGs. One member of the research team (MBF) who participated in all steps of this study is also a PCP working in a FMG. The response rate and presence of most professional titles in each round were acceptable for this study design [ 48 , 49 ], especially considering that professionals’ availability was more challenging due to the ongoing COVID-19 pandemic at the time of data collection. Also, even though the FMG model is specific to the province of Quebec, Canada, it is merely a variation of many other primary care models elsewhere in Canada and worldwide as it is a team-based approach in which primary care professionals (mostly PCPs and RNs supported by other first line professionals) provide longitudinal continuous general healthcare services [ 12 ]. Therefore, we think that the validated tool could easily be adapted and implemented in other similar settings. Another limit to our study is that no patient was part of the research team. This means that even though the decision support tool was validated by health professionals, it might not be well adapted to DFU patients’ needs. This perspective could however be addressed in the future in a patient-oriented research project, and the tool adapted to the findings of such a study.

This study describes the development process and validation of a decision support tool to guide primary care professionals manage DFUs based on current practice guidelines through a modified Delphi protocol. Our tool is all at once a checklist of actions that need to be taken by different professionals, a care pathway and a quick read reference for professionals to be informed about recommended treatments and expected outcomes at different steps along the continuum of care. We believe that it has the potential to contribute to standardizing and to optimizing the provision of care for people with DFUs in primary care. The implementation and evaluation of the tool in the clinical setting will be undertaken as a next step to determine if its use impacts on users’ satisfaction both for professionals and patients, as well as on clinical outcomes.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

• Diabetic foot ulcer

Family medicine group

Registered nurse

Primary care physician

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Acknowledgements

The authors thank Pierre-Luc Yao, PhD, Université du Québec à Trois-Rivières for his contribution with the data analysis. Mr. Yao received no financial support for his participation. They also thank Frédérique Beauchamp for the graphic design. Ms. Beauchamp was compensated for her work.

This work was supported by the Chaire Docteur Sadok Besrour en médecine familiale affiliated with the University of Montreal Faculty of Medicine and Research Center.

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Magali Brousseau-Foley, Virginie Blanchette & François Trudeau

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M.B.F. was responsible for the concept and design of the study, the acquisition of data analysis and interpretation, the writing of the first draft and the critical revision for important intellectual content. V.B., J.H. and F.T. revised the article critically for important intellectual content. All authors contributed to the design of the decision support tool. All authors gave the final approval of the version to be published. M.B.F. is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

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Questionnaires developed by the research team for all three Delphi rounds in translated English language versions.

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Final version of the decision support tool in colors translated to English.

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Original French version of the final version of the decision support tool.

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• Published: 28 April 2024

Impact of shear stress on sacral pressure injury from table rotation during laparoscopic colorectal surgery performed in the lithotomy position

• Kyota Tatsuta 1 ,
• Mayu Sakata 1 ,
• Kosuke Sugiyama 1 ,
• Tadahiro Kojima 1 ,
• Toshiya Akai 1 ,
• Katsunori Suzuki 1 ,
• Kakeru Torii 1 ,
• Yoshifumi Morita 1 , 2 ,
• Hirotoshi Kikuchi 1 ,
• Yoshihiro Hiramatsu 1 , 3 ,
• Kiyotaka Kurachi 1 &
• Hiroya Takeuchi 1  

Scientific Reports volume  14 , Article number:  9748 ( 2024 ) Cite this article

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• Gastroenterology
• Gastrointestinal diseases

This study aimed to evaluate the impact of shear stress on surgery-related sacral pressure injury (PI) after laparoscopic colorectal surgery performed in the lithotomy position. We included 37 patients who underwent this procedure between November 2021 and October 2022. The primary outcome was average horizontal shear stress caused by the rotation of the operating table during the operation, and the secondary outcome was interface pressure over time. Sensors were used to measure shear stress and interface pressure in the sacral region. Patients were divided into two groups according to the presence or absence of PI. PI had an incidence of 32.4%, and the primary outcome, average horizontal shear stress, was significantly higher in the PI group than in the no-PI group. The interface pressure increased over time in both groups. At 120 min, the interface pressure was two times higher in the PI group than in the no-PI group (PI group, 221.5 mmHg; no-PI group, 86.0 mmHg; p  < 0.01). This study suggested that shear stress resulting from rotation of the operating table in the sacral region by laparoscopic colorectal surgery performed in the lithotomy position is the cause of PI. These results should contribute to the prevention of PI.

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Introduction.

Pressure injury (PI) causes occlusion of blood flow and can affect the skin, soft tissue, muscle, and bone. It leads to the development of localized ischemia, tissue inflammation, tissue anoxia, and necrosis 1 . Surgery is a risk factor for PI 2 . Surgery-related PI is reportedly caused by pressure, shear stress, or friction tissue forces, which can occur because of prolonged periods of immobility during an operation 2 , 3 . Surgery-related PI leads to longer hospital stays and higher hospital costs 4 , 5 .

The rate of surgery-related PI differs according to the surgical position. The lithotomy position is recognized as a high-risk position for surgery-related PI 6 , 7 . In recent years, laparoscopic and robot-assisted colorectal surgeries have become common 8 , 9 , 10 . Laparoscopic or robot-assisted surgery performed in the lithotomy position requires the utilization of positioning devices and rotation of the operating table. Rotation of the operating table can cause shear stress 11 . Therefore, the risk of surgery-related PI is expected to increase further when rotation of the operating table is added to the lithotomy position. Several reports have shown surgery-related PI caused by shear stress due to the rotation of the operating table 12 , 13 . However, no studies have specifically investigated the effect of shear stress due to the rotation of the operating table on surgery-related PI.

We hypothesized that shear stress associated with the rotation of the operating table is strongly related to the cause of surgery-related PI in laparoscopic colorectal surgery performed in the lithotomy position. Several areas of the body are considerably affected by PI. The most common postoperative sites where PI is reported to occur are the occipital skull, scapula, elbows, sacral region, and heels. Surgery-related PI in the sacral region is more likely to be fatal 14 . This study aimed to evaluate the impact of shear stress on surgery-related PI in the sacral region by laparoscopic colorectal surgery performed in the lithotomy position.

Study design and patient population

This prospective cohort study recruited and enrolled all patients who underwent laparoscopic colorectal surgery in lithotomy position between November 2021 and October 2022. Among these, we excluded loop colostomy, which does not require rotation of the operating table, and total proctocolectomy, which requires various directions or angles of rotation of the operating table in a single surgery. Robotic-assisted surgery was excluded as it was in the introductory phase. The study design was approved by the Institutional Review Board of Hamamatsu University School of Medicine (IRB number: 20-226) and registered in UMIN-CTR Clinical Trial Registry (UMIN000051051). All methods were performed in accordance with the relevant guidelines and regulations. Written informed consent was obtained from all patients whose physical characteristics were assessed.

Pressure and shear force sensors (Nissha Co., Ltd., Kyoto, Japan) were used to measure the horizontal and interfacial pressures in the sacral region. This sensor can measure an area of 44 mm × 66 mm (11 × 11 cells) every 0.01 s. Changes in the pressure values were recorded consecutively and saved as numeric data. After the lithotomy position, the sensor was placed on top of the positioning devices and pressure redistribution urethane foam (Fig.  1 ). The surgical team measured and recorded the horizontal and interface pressure distributions in the sacral region in both the flat and tilted positions during the operation. The tilt was 15° in the lower-head position and 15° in the lower-right position, and the position was continued for 120 min. After returning to the flat position for 5 min, the operating table was repositioned. This series of the rotation of the operating table was repeated until the surgical procedure was completed. This protocol was determined in accordance with our previous study to prevent well-leg compartment syndrome 15 . The recording time was defined as the time from the start of surgery to bowel resection to minimize getting the sensor soiled by the surgical procedure.

The method of setting up the pressure and shear stress sensor. After the lithotomy position, the sensor is set in alignment with the patient’s sacral region.

Definition of PI in the sacral region

PI was evaluated in the operating room immediately after surgery by multiple members of the surgical team for redness in the sacral region. Patients with skin redness were defined as the PI group. The PI group included patients with pressure ulcers (non-blanchable redness) and reactive hyperemia (blanchable redness). Pressure ulcer was classified based on the National Pressure Ulcer Advisory Panel (NPUAP) 16 . In cases of pressure ulcers, treatment was continued based on the international clinical practice guidelines for the prevention and treatment of pressure ulcers and injuries 17 .

Analysis of horizontal pressure, interface pressure, and shear stress

The force data of the tri-axes are defined as “X-axis” for the lateral pressure within horizontal direction, “Y-axis” for the longitudinal pressure within horizontal direction, and “Z-axis” for the interface pressure. The vector component was calculated from the numerical data of the X, Y, and Z axes of each cell. The direction of the horizontal pressure was calculated as the fundamental unit vector and represented the direction of the arrow. On the X-axis, positive corresponds to the left side and negative to the right side; on the Y-axis, positive corresponds to the foot side and negative to the head side. The horizontal shear stress was calculated as the difference between adjacent cells. These analyses were performed for each cell, four areas (4 × 4 cells), and the entire area.

Outcome measurements

The primary outcome was the average horizontal shear stress in the head and right-down tilt position during the operation. Secondary outcomes were the direction for horizontal pressure in the sacral region, the change over time in horizontal shear stress and the interface pressure in the sacral region. The change over time was evaluated in the flat position, and the head and right-down tilt positions were evaluated every 30 min up to 120 min. Additional secondary outcomes included pre-operative patient characteristics and intra-operative outcomes. In the preoperative patient’s characteristics, the areas of abdominal visceral fat, subcutaneous fat, and psoas major muscle were calculated from a computed tomography (CT) image acquired at the level of L3 using SYNAPSE VINCENT (Fujifilm, Japan). Skin and subcutaneous tissue thicknesses were measured at the thinnest part of the sacral region. The prognostic nutritional index (PNI) was calculated as 10 × serum albumin (g/dL) + 0.005 × total lymphocyte counts (per mm 3 ) 18 . As a post-hoc analysis, we evaluated the distribution of shear stress over the entire area.

Statistical analyses

Statistical analyses were performed using JMP® 16 software (SAS Institute Inc., Cary, NC, USA). The distribution features are presented as mean ± standard error (SE) or median and interquartile range (IQR) for variables with skewed distribution or frequency (proportion [%]). The medians and ranges were calculated, and differences were identified using the Mann–Whitney U test. Categorical data were expressed as frequencies and proportions and analyzed using Fisher’s exact test. Cosine similarity was used to compare the horizontal pressure direction. The cosine similarity is normalized to a range of -1 to 1, where 1 indicates that the horizontal pressure directions are perfectly similar, and -1 indicates that they are not perfectly similar. Statistical significance was set at P  < 0.05.

During the enrollment period, 37 of the 38 patients were included and divided into 2 groups, with or without the presence of PI. One patient was excluded owing to sensor failure. The characteristics and intraoperative outcomes of the study participants are summarized in Table 1 . The incidence of PI was 32.4% (pressure ulcer, 1; reactive hyperemia, 11). No differences were observed in clinical characteristics and intraoperative outcomes. In 83.8% of cases (PI group: 91.7%, no-PI group: 80.0%), surgery was completed within 120 min from the start of the tilt position.

Characteristics of PI

PI mainly occurred on the right sacral region (Fig.  2 ). All patients with reactive hyperemia showed improvement in redness the following day. One case of pressure ulcer was treated with white petrolatum and healed within 3 days.

The site of occurrence of surgery-related pressure injury. ( a ) The representative pressure ulcer and reactive hyperemia cases are shown. ( b ) Each case mapped the center of the site of occurrence of surgery-related pressure injury.

Primary endpoint

Table 2 lists the results for the horizontal shear stress. The average horizontal shear stress in the head and right-down tilt position during the operation was significantly higher in the PI group than in the no-PI group on both the X and Y axes. A post-hoc analysis in which the distribution of shear stress over the entire area showed the PI group was higher shear stress on the right side of the sacral region (Fig.  3 ).

Horizontal shear stress in the sacral region. Heatmap of shear stress over the entire sacral region, rated from 0 to 100 mmHg. The change over time up to 120 min from the start of the tilt position was evaluated. PI, pressure injury.

Secondary endpoint

Direction for horizontal pressure for in the sacral region.

Figure  4 shows the direction of the horizontal pressure over time. In the no-PI group, the component of the longitudinal pressure in the horizontal direction was strong in each region, and most of the horizontal pressure was directed toward the head side. In contrast, in the PI group, the horizontal pressure was directed toward the right temporal direction in areas 1, 2, and 3, but toward the left temporal direction only in area 4. For the no-PI group, a correlation was noted in the horizontal pressure direction in all areas at all times. However, the PI group had correlations between areas 1 and 3, whereas area 4 had no correlation with the other areas in the horizontal direction.

Direction for horizontal pressure for in the sacral region. The direction of horizontal pressure was analyzed in four separate areas (4 × 4 cells). The change over time up to 120 min from the start of the tilt position was evaluated. The similarity of vector components for each region was evaluated using cosine similarity over time. PI, pressure injury.

The change of horizontal shear stress over time

Over time, the shear stress on the Y-axis was significantly higher in the PI group at all times. The shear stress on the X-axis was statistically different from 90 min onward (Table 2 ).

Interface pressure in the sacral region

Figure  5 a shows a heat map of the interface pressure changes over time in the sacral region. The interface pressure increased over time in both groups. In the no-PI group, the interface pressure increased uniformly in all areas. However, in the PI group, the interface pressure increased dramatically in areas 1 and 3, whereas no increase in pressure was observed in areas 2 and 4. Figure  5 b shows the numerical data of the changes in the interface pressure over time in each area. In areas 1 and 3, the PI group showed significantly higher interface pressure than the no-PI group 60 min after the start of lithotomy position, followed by a more dramatic increase. At 120 min after the start of the lithotomy position, the interface pressure was twice as high in the PI group as in the no-PI group (PI group, area 1: 221.5 mmHg; no-PI group, area 1: 86.0 mmHg; p  < 0.01).

Interface pressure in the sacral region. ( a ) Heatmap of interface pressure over the entire sacral region, rated from -100 to 100 mmHg. ( b ) Interface pressure was analyzed in four separate areas (4 × 4 cells). Median ± standard error values were represented. * p  < 0.05, ** p  < 0.005, *** p  < 0.0005. PI, pressure injury.

This was a prospective observational study investigating the impact of shear stress on surgery-related PI in laparoscopic colorectal surgery performed in the lithotomy position. The shear stress was significantly higher in the PI group and tended to be higher on the right side of the sacral region. Moreover, the PI group showed twice as much interface pressure in the sacral region as the no-PI group. This is the first study to demonstrate the impact of shear stress in the sacral region in the lithotomy position on the occurrence of surgery-related PI. This study significantly contributes to the prevention of surgery-related PI.

The effect of shear stress on the development of pressure ulcers has been widely reported 19 . However, previous studies on the relationship between shear stress and PI have been limited to the quantitative measurement of pressure and shear stress on the body of wheelchair users 20 , 21 or on foot ulcers in patients with diabetes mellitus 22 , 23 , 24 . No reports have evaluated the relationship between surgery-related PI and shear stress. As we hypothesized, shear stress due to the rotation of the operating table, the primary endpoint of this study, was shown to significantly impact surgery-related PI. According to past reports, a shear stress of 3.1 kPa (approximately 23.3 mmHg) applied to the sacral region affects blood flow reduction in the sacral region 21 , 25 . In the present study, the average X and Y axes values were as high as 26.1 mmHg and 33.3 mmHg, respectively. The bias in the direction of the horizontal pressure in each area is considered the cause of the shear stress development. This bias started at the beginning of the tilt position and continued over time. The shear stress, especially on the Y-axis, was significantly greater in the PI group over time from the beginning of the tilt position. In addition, both the sites of high shear stress and occurrence of surgery-related PI were on the right side of the sacrum. Further, this result indicates that shear stress affects surgery-related PI.

Regarding the interface pressure, the results were also strongly influenced by the rotation of the operating table. The results of a previous study on interface pressure in the lithotomy position without rotation showed that the interface pressure was 93.3 mmHg in the sacral region over time 7 . In our study, the interface pressure in the sacral region of the no-PI group ranged from 68.4 to 110 mmHg. Surprisingly, the PI group showed a left–right difference in interface pressure in the sacral region, with the right side of the sacral region being > 200 mmHg. Previous studies have shown that the primary cause of pressure ulcers is ischemia produced by external pressures greater than capillary pressure (12–32 mmHg), and a constant pressure of 70 mmHg applied for 2 h produced ischemic changes 26 , 27 , 28 . In the PI group, an interface pressure > 200 mmHg on the right side of the sacral region was extremely abnormal. Similar to the mechanism of shear stress development, the bias in the direction of the horizontal pressure by each area is considered to be the cause of interface pressure development. We believe that it is crucial to elucidate the reason for the bias in the direction of the horizontal pressure.

Considering that the same positioning devices are used in all surgeries, we assume that this bias may reflect differences in the orientation and tilt of the patient’s body axis that occur when using positioning devices or that are caused by the patient’s body balance. Generally, the nutritional status, a history of diabetes mellitus, a high body mass index, prolonged surgery, and massive blood loss are considered risk factors for surgery-related PI 2 , 29 , 30 . The present study examined results of these previous studies using an index reflecting nutritional and body mass indexes in detail. We used PNI for nutritional indices 31 and L3 levels of visceral fat, subcutaneous fat, and the psoas major muscles for high body mass index 32 . However, no difference was found in the clinical characteristics and intraoperative outcomes. There may be reasons for the occurrence of surgery-related PI specific to laparoscopic or robot-assisted surgery in the lithotomy position.

The incidence of surgery-related PI in this study was found to be 32.4%, which was higher than the incidence of PI in the lithotripsy position reported to be 25.9% in a previous study 33 . The incidence of PI in this study was probably higher because this study was limited to laparoscopic colorectal surgery with rotation of the operating table. On the other hand, the frequency of pressure ulcer was 2.7%, which was lower than that reported previously 34 . However, the frequency of surgery-related PI in the lithotomy position is much higher than the general incidence of surgery-related PI (6.3%) 3 . Thus, various preventive measures should be taken to reduce surgery-related PI in the lithotomy position.

Although this study showed that shear stress is associated with surgery-related PI, we were not able to make any recommendations regarding preventive measures for such injuries. A recent systematic literature review indicates that PI risk assessment and pressure redistribution using dressings are recommended 35 . In addition, recent clinical trials have examined the type of dressing material and showed that multi-layered silicone foam is more efficacious than transparent polyurethane film in preventing PI caused by surgical positioning 36 . Further research specific to the lithotomy position is desirable based on these preventive measures.

Our study had several limitations. First, it was a single-center study with a small sample size. Our participants represented a specific patient population, thus limiting the generalizability of our findings. Future studies with larger sample sizes should be conducted to confirm the results of this study and explore the effects of shear stress and interface pressure over longer periods. Second, the analysis in this study was limited because it was not performed for the entire lithotomy position. However, since only one patient (8.3%) in the PI group returned to the flat position and performed a second tilt position, we did not believe that this would significantly affect the results of this study. Third, we examined cases of laparoscopic surgeries performed in the lithotomy position that required rotation of the operating table. Therefore, the results of this study cannot be applied to cases that do not require rotation or that are rotated in different directions or angles. Fourth, this study did not consider other factors associated with pressure ulcers, such as perfusion, oxygenation, skin moisture, and body temperature. The influence of tissue damage differs by the tissue type and may be influenced by microclimate, perfusion, systemic comorbidities, and localized conditions of soft tissues, which are affected by sustained mechanical loading 37 . Therefore, a prospective study that includes various factors involved in PI development is required to validate the present study's results.

This study provides evidence that shear stress in the sacral region due to rotation of the operating table in laparoscopic colorectal surgery performed in the lithotomy position is the cause of surgery-related PI. These results emphasize a contribution towards the prevention of surgery-related PI.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors would like to thank all the patients, medical staff at the institution, and the members of Nissha Co., Ltd., who contributed to this study. We are grateful to Mikihiro Shimizu, Center for Clinical Research, Hamamatsu University School of Medicine, for the helpful statistical analysis.

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Kyota Tatsuta, Mayu Sakata, Kosuke Sugiyama, Tadahiro Kojima, Toshiya Akai, Katsunori Suzuki, Kakeru Torii, Yoshifumi Morita, Hirotoshi Kikuchi, Yoshihiro Hiramatsu, Kiyotaka Kurachi & Hiroya Takeuchi

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K.T. wrote the manuscript, was involved in data collection, and performed the analysis. M.S., K.K. and K.S. conceived and designed the analysis, and critically revised the report. K.S., T.K., T.A. and K.T. were involved in data collection and performed the analysis. Y.M., H.K., Y.H. and H.T. critically revised the report and commented on the drafts of the manuscript. All authors read and approved the final manuscript.

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Tatsuta, K., Sakata, M., Sugiyama, K. et al. Impact of shear stress on sacral pressure injury from table rotation during laparoscopic colorectal surgery performed in the lithotomy position. Sci Rep 14 , 9748 (2024). https://doi.org/10.1038/s41598-024-60424-9

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Mediterranean Diet Linked to Lower Hypertension Risk, Study Finds

This eating plan just added another benefit to its resumé.

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• New research finds that the Mediterranean diet helps lower hypertension risk.
• The study followed participants for 20 years before determining the effects of the diet.
• Experts explain the Mediterranean diet’s heart health benefits.

A study published in the European Journal of Clinical Nutrition looked at the cardiovascular advantages of the Mediterranean diet. Researchers analyzed data spanning 20 years and found that people who consistently followed a Mediterranean-style diet had a lower risk of developing hypertension (high blood pressure) than those who did not adhere to the diet as closely.

The study occurred in 2002 through 2022, and involved 3,042 participants who were not hypertensive at the beginning. The researchers collected a variety of information on the participants at the start, including glucose and cholesterol levels, body weight, and blood pressure. To see how closely the participants followed the Mediterranean diet at the beginning of the study, they were assigned a MedDietscore based on eating the following food groups: fruits, vegetables, whole grains, potatoes, legumes, fish, and olive oil. Over 20 years, researchers followed up with the participants to assess their MedDietScore and to check for the development of hypertension, high cholesterol , type 2 diabetes , and cardiovascular disease.

The study found that participants who closely adhered to the Mediterranean diet had the lowest risk of developing hypertension. The group with the highest MedDietScore, who followed the Mediterranean diet the best, had a hypertension incidence rate of 8.7%. In comparison, participants in the group who had the lowest MedDietScore—and therefore followed the diet less closely—had hypertension rates of 35.5% by the end of the study.

Researchers also wanted to evaluate how following the diet consistently impacted hypertension risk. They found that those who were closely adhering to the Mediterranean diet regularly exhibited a 46.5% lower 20-year hypertension risk compared to those who were frequently not following the diet.

So what about the Mediterranean diet makes it great for regulating blood pressure and optimizing heart health? The answer may lie in a specific nutrient. Typically, meal patterns that include potassium-rich foods (like fruits, vegetables, and legumes) are beneficial for keeping your blood pressure in check, says Melissa Prest, D.C.N., R.D.N. , national media spokesperson for the Academy of Nutrition and Dietetics and member of the Prevention Medical Review Board . “The Mediterranean diet is a great example of a meal pattern that includes these foods and is lower in saturated fat and sugar.”

When following a Mediterranean diet, you’ll generally get plenty of veggies and fruits that offer dietary fiber , potassium, and magnesium , all of which are associated with healthy blood pressure, adds Jackie Newgent, R.D.N., C.D.N. , chef, nutritionist, and author of The Plant-Based Diabetes Cookbook . Plus, “you’ll be able to enjoy liberal use of olive oil , which is also linked to lowered blood pressure.”

Compared to a standard American diet, people following a Mediterranean diet are consuming more minimally processed foods , plant foods, fiber, and healthy fats, explains Prest. “This mix is important when eating to maintain normal blood pressure.” If you are at risk for high blood pressure and want to adopt Mediterranean diet principles, consider adding fruits and vegetables to most meals and snacks, mix up your protein by choosing plant proteins more often, and savor sweets and red meat as an occasional treat, Prest advises.

The bottom line

We know that the Mediterranean diet is often recommended for overall heart health, but this new research specifically shows the benefits of following the eating pattern in those with high blood pressure. This study showed that long-term adoption of the Mediterranean diet has a big impact on reducing high blood pressure risk, says Prest. Newgent agrees that it’s not about a quick-fix diet, and these results suggest that following the eating pattern long-term is advised for better heart health.

In general, people with high blood pressure can benefit from following a Mediterranean-style diet with the addition of consuming less salt and alcohol, advises Prest. With that said, if someone needs to avoid food like nuts, for instance, or curb a nutrient such as potassium, that’s prevalent on a Mediterranean diet, they may simply need to follow a modified, personalized version of it, says Newgent. Also, if there are health concerns, like low blood pressure , work with a registered dietitian nutritionist to help you tweak the diet to address those concerns, says Prest.

Madeleine, Prevention ’s assistant editor, has a history with health writing from her experience as an editorial assistant at WebMD, and from her personal research at university. She graduated from the University of Michigan with a degree in biopsychology, cognition, and neuroscience—and she helps strategize for success across Prevention ’s social media platforms. 

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• Published: 24 April 2024

How does atmospheric pressure cold helium plasma affect the biomechanical behaviour on alkali-lesioned corneas?

• Simona Neri 1   na1 ,
• Maria Vittoria Mascolini 2 , 3   na1 ,
• Antonella Peruffo 4 ,
• Silvia Todros 2 , 3 ,
• Matteo Zuin 5 , 6 ,
• Luigi Cordaro 5 , 6 ,
• Emilio Martines 7 ,
• Barbara Contiero 1 ,
• Emanuele Luigi Carniel 2 , 3 ,
• Ilaria Iacopetti 1 ,
• Marco Patruno 4 ,
• Chiara Giulia Fontanella 2 , 3   na2 &
• Anna Perazzi 1 , 3   na2  

BMC Veterinary Research volume  20 , Article number:  153 ( 2024 ) Cite this article

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Melting corneal ulcers are a serious condition that affects a great number of animals and people around the world and it is characterised by a progressive weakening of the tissue leading to possible severe ophthalmic complications, such as visual impairment or blindness. This disease is routinely treated with medical therapy and keratoplasty, and recently also with alternative regenerative therapies, such as cross-linking, amniotic membrane transplant, and laser. Plasma medicine is another recent example of regenerative treatment that showed promising results in reducing the microbial load of corneal tissue together with maintaining its cellular vitality. Since the effect of helium plasma application on corneal mechanical viscoelasticity has not yet been investigated, the aim of this study is first to evaluate it on ex vivo porcine corneas for different exposition times and then to compare the results with previous data on cross-linking treatment.

94 ex vivo porcine corneas divided into 16 populations (healthy or injured, fresh or cultured and treated or not with plasma or cross-linking) were analysed. For each population, a biomechanical analysis was performed by uniaxial stress-relaxation tests, and a statistical analysis was carried out considering the characteristic mechanical parameters. In terms of equilibrium normalised stress, no statistically significant difference resulted when the healthy corneas were compared with lesioned plasma-treated ones, independently of treatment time, contrary to what was obtained about the cross-linking treated corneas which exhibited more intense relaxation phenomena.

Conclusions

In this study, the influence of the Helium plasma treatment was observed on the viscoelasticity of porcine corneas ex vivo, by restoring in lesioned tissue a degree of relaxation similar to the one of the native tissue, even after only 2 min of application. Therefore, the obtained results suggest that plasma treatment is a promising new regenerative ophthalmic therapy for melting corneal ulcers, laying the groundwork for further studies to correlate the mechanical findings with corneal histology and ultrastructural anatomy after plasma treatment.

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Corneal ulcers affect a great number of people and animals worldwide every year and can lead to severe complications such as visual impairment or blindness when not properly treated [ 1 ]. In particular, treating melting infectious keratitis, a condition that implies an imbalance between proteinases and proteinases inhibitors, is becoming increasingly harder. This disease can develop very quickly, even in 24–48 h, triggered and carried on by many types of bacteria, fungi and viruses, such as Pseudomonas spp., Staphylococcus spp., Candida spp., Acanthamoeba spp. and Herpes spp [ 1 ]. These microorganisms, together with host activated leukocytes, produce many proteolytic enzymes that can damage and dissolve the corneal stroma, potentially leading to its perforation if not properly regulated [ 2 ]. The difficulty in coping with this condition is due to the frightening growth of antibiotic resistance, the increased need of cornea donors, and the rise in the costs of medical and surgical therapies. So, great efforts in regenerative medicine research focus on developing reliable and affordable alternatives to keratoplasty, such as corneal cross-linking (CXL) [ 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 ], stem cells transplant [ 14 , 15 , 16 , 17 , 18 ], platelet-rich plasma [ 19 , 20 ], argon laser [ 21 ]. Another emerging regenerative treatment is plasma medicine [ 22 ]. Plasma medicine makes use of an ionised gas (plasma) directly on biological tissues for therapeutic purposes. Helium, argon, oxygen, nitrogen, or a mixture can be used. The gas flow is ionised passing through an electric field, which induces the gas breakdown and the formation of a low temperature plasma (here the temperature is that of the neutral gas, which remains the dominant component), generating many reactive oxygen and nitrogen species (ROS and RNS). The spreading of these species directly on the surface of damaged tissue improves the healing process by inactivating microorganisms and stimulating cells to produce proinflammatory cytokines and neoangiogenic factors [ 23 , 24 , 25 ]. Plasma medicine has been investigated in human skin wound healing in experimental trials on volunteers [ 23 ] and in ex vivo human corneas [ 26 , 27 , 28 ]. Martines et al. [ 27 ] studied the efficacy and safety of a 2 min exposure of human ex vivo corneas to helium cold plasma flow. They showed a ROS-induced antimicrobial effect of the treatment, without any DNA damage in keratocytes and conjunctival fibroblasts and without modifications on corneal cells viability, demonstrating that the use of plasma could be an effective tool for infectious keratitis management. As the main problem of melting corneal ulcers is the softening of the tissue and the modifications in its mechanical functionality that can lead to eyes perforation, the goal of medical research should be the design of a method that strengthens the structure of the corneal stroma. So, it is important to investigate the corneal biomechanical properties in physiological conditions, their changes in tissue strengthening due to melting lesions and different treatments.

Biomechanical tests can be performed on ex vivo porcine corneas that have been already frequently used as a model to estimate the eyes properties of humans and other animals [ 29 , 30 , 31 ], despite some differences in thickness between species. Uniaxial tensile tests and inflation tests are the most used methods for ex vivo studies [ 29 , 31 , 32 , 33 , 34 , 35 ]. The literature reports few studies on this aspect and with contrasting outcomes [ 23 , 35 , 36 , 37 ]. Biomechanical evaluation of corneal tissue properties after helium cold plasma exposition is missing in the literature, while it has been investigated for other treatments, such as cross-linking by Fontanella et al. [ 38 ]. The above-mentioned paper assessed the biomechanical properties of the corneal tissue of ex vivo healthy versus alkali-induced lesioned porcine corneas treated/not treated with CXL, showing a surprising weakening of the lesioned populations despite the treatment [ 38 ], a result that is in contrast with the literature.

Indeed, corneal cross-linking has been demonstrated to be effective for the treatment of human and animal collagenasic corneal ulcers, because it seems to increase the stiffness and the resistance of the cornea. This effect is due to a photochemical reaction occurring when the corneal stroma is soaked with riboflavin (Vit. B2) and then radiated with UVA. This interaction generates free oxygen radicals with antimicrobial properties and develops new covalent bonds in the collagen fibrils of the stroma, reinforcing the tissue and influencing its biomechanical functions [ 29 , 31 , 32 , 33 , 34 , 35 , 36 ]. CXL was originally designed for human keratoconus and then, due to its antimicrobial effects, was applied to infectious keratitis [ 3 , 4 , 5 , 6 , 7 , 8 ], also in veterinary ophthalmology [ 9 , 10 , 11 , 12 , 13 ].

So, considering the potential use of plasma medicine for ophthalmic purposes as an alternative to traditional therapies, this study has a twofold purpose. The first aim is to evaluate how the exposition to the ROS produced in a helium plasma modifies the biomechanical properties of the corneal tissue by considering two treatment times and the same experimental conditions and mechanical protocol as the study on CXL [ 38 ] The second and collateral aim is to compare the results with those published on CXL treatment [ 38 ], in order to assess if there is any difference in corneal tissue relaxation after the two types of processing.

Porcine organ-culture preparation procedure

A total number of 52 corneal samples were successfully set up, found clear and without corneal scarring, opacities or injuries. The plasma treatment was correctly performed in all of the samples. All the corneas were stored in the liquid medium for preservation and did not develop any oedema or infection over the period of cultures (7 days). The same condition was observed in the healthy, lesioned and CXL-treated corneal population, as already described in Fontanella et al. [ 38 ] thus allowing to join all data for the statistical analysis and the comparison of mechanical behaviour. The populations setting is described in Table  1 .

Mechanical testing results

Stress-strain behaviour.

The equilibrium stress-strain curves of each group were compared. The median curves for each population are represented by coloured lines and the surrounding coloured area represents the dispersion of the data group (Fig.  1 ). All the curves show a stiffening trend, so a non-linear behaviour of the corneal tissue. The slope of the curve depends on the tissue stiffness: the greater the steepness of the curve, the higher the tissue stiffness. The induction of a lesion resulted in a lower stiffness if compared to the healthy group, under the same other experimental conditions (Fig.  1 a). Moreover, the preservation of corneas in a culture medium resulted in a weakening of the tissue if compared to fresh corneas on equal other conditions (Fig.  1 b). The in-culture groups displayed lower values compared to their counterpart fresh ones, except for the LCP4 group which showed higher values (unexpected result). In terms of the exposure time to the plasma treatment (Fig.  1 c), the HFP2 group showed lower values of stiffness compared to the HFP4.

Stress-strain curves at equilibrium resulted for plasma-treated corneas in case of ( a ) induction of lesion, ( b ) culture preservation and different exposition times for ( c ) healthy corneas and ( d ) lesioned corneas. Median curves are reported together with 50% probability scatter bands

Viscoelastic behaviour

The stress-relaxation curves show a decrease of normalized stress with time, while a constant strain is applied. This time-dependent behaviour is typical of viscoelastic soft tissues. In all data groups, the stress reaches a plateau in the time range of 400 s. As for the stress-strain curves, the median curves for each population are represented by coloured lines and the associated coloured area represents the range of data dispersion within the group. As concerns the relaxation behaviour, by comparing healthy versus lesioned (Fig.  2 a) and fresh versus cultured (Fig.  2 b) plasma-treated corneas, no effect of lesion and culture preservation was found. Moreover, the exposition to plasma treatment for 2 or 4 min induced similar stress relaxation over time (Fig.  2 c, d).

Normalized stress-relaxation curves resulted for plasma-treated corneas in case of ( a ) induction of lesion, ( b ) culture preservation and different exposition times for ( c ) healthy corneas and ( d ) lesioned corneas. Median curves are reported together with 50% probability scatter bands

Particular attention was focused on the four populations representing the most typical realistic situation: corneas which were lesioned, cultured and plasma-treated with two different exposition times, namely 2 and 4 min. These results were compared to the behaviour exhibited by healthy untreated fresh corneas and by lesioned CXL-treated corneas (Fig.  3 ). The comparison was done under the same stress-relaxation protocol. Considering the stress-strain behaviour, the HFN group showed the highest values of stiffness. Comparing the plasma and cross-linking treatment, LCP4 groups showed slightly higher stress values than LCY (Fig.  3 a). Considering stress relaxation phenomena, the plasma-treated corneas for both exposition times exhibited a time-dependent behaviour similar to the native tissue (Fig.  3 b), contrary to the corneas treated with CXL. The relaxation intensity observed in the plasma-treated (2 and 4 min) groups (F, C, L) are very similar, whereas, comparing the plasma and cross-linking treatment, more intense relaxation phenomena are observed in the LCY group.

Lesioned plasma-treated in culture corneas results compared to the behaviour of healthy untreated fresh corneas and lesioned CXL-treated in culture corneas. ( a ) Stress-strain curves at equilibrium and ( b ) relative stress-relaxation curves reported in terms of median and associated 50% probability scatter bands

The in-culture groups displayed very similar properties to their counterpart fresh ones for 2 min plasma treatment in both healthy and lesioned conditions, while fresh 4 min-plasma treated corneas showed lower values of relaxed stress at the end of the experimental tests, if compared to the in-culture ones (HCP4, LCP4).

Statistical analysis results

From the equilibrium stress-strain curves, the tangent modulus was calculated referring to two different regions, namely the toe and linear regions, for the different groups. The analysis of variance for the toe region parameter revealed that, the healthy population whether consisting of cultured or fresh samples, exhibited a significantly higher values compared to all the other treatment groups, whether considering fresh or cultured and healthy or lesioned samples (Fig.  4 a). Notably, among all control groups, HFN had the highest values (1.19 ± 0.71 MPa). Regarding the linear region parameter, the groups’ effect was again significant in the ANOVA analysis primarily driven by HFN which displayed the highest value (9.43 ± 6.82 MPa) and HCN (3.93 ± 1.35 MPa), (Fig.  4 b). These values resulted significantly different from all the other groups.

Bar chart (mean ± SD) representative of the tangent modulus ( a ) in the toe region E1 and ( b ) in the linear region E2 for stress-strain curves and ( c ) the parameter γ ∞ for normalized stress-relaxation curves

On the other hand, the parameter γ ∞ at the end of the relaxation phase was obtained from stress-relaxation curves. The γ ∞ represents the normalized residual stress, i.e., the ability of the material to relax when a constant deformation is applied over time. This parameter highlights the viscosity of the tissue.

By considering γ ∞ in the different groups, no statistically significant differences were found between the 2 exposure times (2 and 4 min) to the plasma treatment (Fig.  4 c). The degree of relaxation in healthy and lesioned plasma-treated corneas for both the exposure times resulted not statistically different compared to the control group (HFN), independently of the preservation method (fresh/in culture). Under the condition of lesion and culture preservation, the γ ∞ exhibited by the plasma-treated corneas (LCP2 = 0.28 ± 0.01 and LCP4 = 0.27 ± 0.02) resulted significantly higher than the untreated corneas (LCN = 0.17 ± 0.02; P  = 0.002 and P  = 0.012 respectively), as reported in Fig.  4 c. Moreover, comparing the two corneal treatments considered (LCP2 and LCP4 versus LCY), CXL treated groups showed a degree of relaxation significantly higher that the plasma treated (CXL = 0.17 ± 0.01; P  < 0.001 and P  = 0.035 respectively).

In the current literature, plasma treatments have been studied in human corneal cells cultures and donated human corneas under microbiological, regenerative and safety aspects [ 26 , 28 , 39 , 40 , 41 ], without investigating the effect on the viscoelasticity of the tissue. In the present study, the results of stress-relaxation tests carried out on porcine corneas first alkali-lesioned and then treated with plasma confirmed the typical non-linear and time-dependent behaviour of the cornea, reported in literature [ 30 , 31 , 32 , 38 , 42 ].

In addition, the current work demonstrates that the exposure of lesioned corneas to the plasma treatment modifies the biomechanical properties of the corneal tissue, if compared to the injured ones. In particular, the plasma treatment restored the relaxation behaviour of the corneal tissue exhibiting values of the equilibrium normalized stress similar to the native tissue (Fig.  4 c) [ 32 , 34 ]. This result is well highlighted by the parameter γ ∞ that appears to be the same between healthy corneas and those treated with plasma after being damaged.

This viscoelasticity restoration could be the consequence of variations in the chemical components of the corneal stroma after the exposition to the many ROS species that are generated by the plasma flow. In fact, it is well known that ROS are involved in wound healing acting like molecules signals regulators for cell migrations and neoangiogenesis and showing an antimicrobial effect on the tissue [ 23 , 24 , 25 , 27 , 28 , 41 , 39 , 43 ].

This result is favourable to the development of a new treatment for melting corneal ulcers, because it could help in preventing corneal perforation by enhancing the stiffness of the tissue. By weighing up plasma and CXL treatments, the obtained results showed that the cross-linking was less effective in terms of bringing the mechanical properties of the tissue back to original normal values. This outcome could lead ophthalmologists to question the choice of CXL for the treatment of corneal infections in favour of plasma.

However, this study has some limitations, such as the time of the culture that was conducted only for 7 days to prevent corneal infections and ensure the vitality of the tissue (more realistic situation). Further investigations are needed to study if a longer conservation after the plasma and CXL treatments affects the mechanical results. Moreover, this is an ex vivo study, so the influence of regenerative processes, such as neoangiogenesis and cell proliferation, that normally take place in vivo situations could not be considered.

To reduce the bias of this study all the present samples and the previous published ones were strictly managed under the same experimental conditions in different days and with different operators; increasing the number of the samples in future research could be helpful to minimize statistical errors.

In order to better understand how the plasma treatment affects the biomechanical properties of the corneal tissue, inflation tests are under investigation. This biomechanical test can better mimic how the tissue responds to elongation in its normal shape and in multiaxial loading conditions and could add other, more realistic information for further clinical applications.

Moreover, to investigate the anatomical effects of plasma in the corneal tissue, histopathology and ultrastructural analysis will be the next steps of our research, in order to evaluate if plasma treatment leads to higher tissue compactness, as already seen in a previous study on CXL effects [ 44 ]. Indeed, Perazzi et al. [ 44 ] showed by ultrastructural analysis that a higher brightness of a portion of the corneal section examined in that study corresponded to a major damage and a loss of collagen density, while a lower intensity matched a greater stroma compactness. Interestingly, alkali-injured and then CXL treated corneas exhibited brightness values similar to normal tissue ones, suggesting a possible complete recovery after the treatment and demonstrating the ability of riboflavin/UV-A phototherapy to increase stroma collagen.

In human medicine, a histopathologic evaluation of the effect of plasma medicine on organic tissue has been evaluated on the skin, where it has been proved that argon plasma treatment can increase epidermal thickness and dermal collagen density [ 45 ]. Considering the biomechanical results of this paper, that lean to a recovery of corneal stiffness after helium-plasma treatment, similar histopathologic results and corneal collagen restoration will be expected too after plasma application.

According to the above, plasma medicine is a new promising regenerative treatment that can improve and faster corneal healing. As a result of future studies and additional experimental tests, the efficacy and security of helium plasma treatment will be further validated before its applications in vivo in animals and human patients with corneal collagenasic ulcers.

This is the first experimental study that investigates the effects of a helium plasma treatment on the biomechanical properties of ex vivo porcine corneas and it is part of a wider research on the current and the next innovative regenerative medicine techniques. Plasma treatment demonstrated to have an effect on the mechanical properties of the corneal tissue, in terms of increasing its stiffness even after only 2 min of application and recovering the physiological viscoelastic properties of the tissue, suggesting to be a promising possible alternative regenerative treatment to keratoplasty in melting corneal ulcers, by potentially preventing corneal perforation.

52 porcine eyes were collected from an affiliate slaughterhouse close to the University of Veterinary Medicine in Padua, according to Italian and European law (86/609/EEC). As this is an ex vivo study without any animal sacrifice, no ethical approval and review was necessary. All the samples were considered similar because came from animals of the same age, breed and weight at slaughtering. The eyes were stored immediately after enucleation in a 10% povidone iodine solution and shipped refrigerated at 4 °C to the laboratories for being processed.

The samples were equally and randomly divided into eight experimental populations, considering healthy (H) or lesioned (L) corneas, fresh (F) or culture (C) conditions and plasma treatments with different exposure times, namely 2 (P2) and 4 min (P4).

Healthy corneas were tested in their physiological state, whereas lesioned corneas were tested after the exposure of their central portion to a paper filter (0,8 mm) soaked with sodium hydroxide (NaOH) for 1 min to induce an alkali-like experimental lesion, that is chemically comparable to a melting corneal ulcer. The plasma treatment was performed using a plasma source previously described [ 46 ] and tested both in vitro [ 41 ] and in vivo [ 39 ]. The treatment consisted in the close exposure (at a distance equal to 2 mm) of the central portion of the cornea (a circular region of around 1 cm diameter) for 2 or 4 min to a 1.75 L/min helium gas flow passing through a couple of parallel grids driven by a 4.5 MHz radio frequency sinusoidal voltage difference of approximately 1 kV peak-to-peak (Fig.  5 ). The plasma produced between the two grids is enriched in ROS and RNS, due to the air traces which mix with the helium flow. The sample is then exposed to the afterglow. The plasma treatment takes place rinsing with sterile PBS (Dulbecco’s PBS; PAA Laboratories) the surface of the cornea every minute to prevent dryness. Fresh corneas were tested within 6 h from harvest and were maintained soaked in physiologic saline solution at room temperature prior to tests, culture populations after 7 days of preservation in a specific medium (CARRY-C®, Alchimia, Padua) to maintain the native biological characteristics of the tissue. Before being stored as described above, to reduce the risk of tissue contamination, the corneas were isolated from the entire bulbs, maintaining approximately 4 mm of peri-limbal sclera. Then, each sample were suspended into a sterile bottle filled with 25 ml of preservative medium with sutured thread passing through the adjacent sclera and incubated at 37 °C with 5% CO 2 . A daily check was performed during the culture period: if the colour of the medium moved from red to yellow, indicating contamination of the tissue, the sample was eliminated from the study.

Exposition of the cornea to the plasma treatment

Moreover, the results on the biomechanical behaviour of additional 42 porcine corneas previously described and tested [ 38 ] were added to the analysis, thus including also non-treated (N) and CXL-treated (Y) populations (Vetuvir®, vision Engineering Italy srl, Rome, Italy). As comprehensively described in [ 38 ], N corneas didn’t receive any treatment, while the central portion of the Y corneas was wet for 30 min with an isoosmolar 0.1% riboflavin solution (Peschke Traid, Huenenberg, Switzerland) administered in a circular plastic well held in contact with the surface of the tissue to promote the imbibition of the stroma. Then, with a commercially available equipment, the corneas were irradiated at a distance of 10 cm for 3 min with 30mW/cm2 UV-A of 365 nm wavelength and a total energy of 5,4 J/cm2. As for the P populations, a 1 min PBS flush was set at the end of the treatment.

Therefore, the corneas were considered in healthy status, non-treated or after the plasma or CXL treatment in fresh (HFN, HFP2, HFP4, HFY) and culture (HCN, HCP2, HCP4, HCY) conditions and similarly for the lesioned status (LFN, LFP2, LFP4, LFY, LCN, LCP2, LCP4, LCY).

Mechanical tests

From each cornea, a single corneal sample was obtained for mechanical testing. Each sample was trimmed using a specific cutting die for a rectangular shape (width 4 mm, length 10 mm). The corneal samples were cut along the medial/lateral direction, leaving a small amount of sclera for gripping (Fig.  6 a).

( a ) Geometry of corneal specimen for ( b ) mechanical tensile test

The mechanical tester used was a Bose ElectroForce ® Planar Biaxial Test Bench (TA Instruments, New Castle, USA), equipped with a load cell of 22 N. Mechanical tests were carried out following a protocol already described [ 38 ]. Before testing, sample thickness was measured using a digital calliper at different positions, and then each end of the samples was interposed between two patches of balsa wood, to which the male sides of the Velcro were glued. A medical-grade cyanoacrylate glue (Glue Loctite 4013 Prism) was used to fix the ends of the samples on Velcro surfaces. Finally, the samples were positioned within the grips of the mechanical tester, aligned and a closure pressure was adjusted to avoid slippage. During testing, samples were continuously hydrated by dropping the solution on the sample surface (as showed in Fig.  6 b).

All the samples were subjected to a first preconditioning phase through the application of 10 loading-unloading cycles up to 8% strain, at a strain rate of 1%/s. Then, the stress-relaxation protocol included four consecutive steps of almost instantaneous strain (strain rate of 800%/s), with each step of 8% strain, which was held constant for a time interval of 400s .

Post-processing technique

Experimental force-time data, depending on the assumed strain history, were obtained from each test (Fig.  7 ). Force was then converted to stress, as the ratio between force and the initial cross-sectional area. The equilibrium stress-strain curves were obtained considering the end of relaxation phases and the corresponding applied strain, leading to the mechanical response when all the time-dependent phenomena completely occur. The corneal viscoelastic response was analysed considering stress versus time curves. Stress relaxation data were processed by computing the normalized stress as the ratio between the current stress and peak stress of each rest phase [ 38 ] and then, the normalized stress-time curves were separately fitted by the following exponential formulations:

Depending on the ( a ) strain history, typical force-time data measured for the stress-relaxation test. In red the peak loads corresponding to the quasi-instantaneous application of the displacement level while in green the equilibrium loads after 400 s

where parameters γ1,γ2 represent the relative stiffness and τ1,τ2 the time constants of relaxation. From the equilibrium stress-strain curves, two tangent moduli were calculated as the slope of the curve in the toe region ( E1 ) and in the linear region ( E2 ), while for the normalized stress-time curves the attention was focused on the equilibrium region by considering the equilibrium normalized stress γ∞, computed as:

Statistical analysis

For the statistical analysis, all of the corneal samples described in the methods section were included. Totally, 94 samples from 16 levels were considered from the combination of 3 factors: healthy versus lesioned (population factor: 2 levels), culture versus fresh (condition factor: 2 levels), N versus P2 versus P4 versus Y (treatment factor: 4 levels). The regression between stress-strain or stress relaxation and time were analysed using a non-linear model. Two parameters of the stress-strain curves (E1 toe region and E2 linear region) and one of the relaxation curves (γ ∞ , plateau of the curve) were calculated. The parameters estimated for the 94 individual curves were subjected to ANOVA, considering the fixed effect of the 16 combined levels. Post-hoc pairwise comparison among levels was performed using the Bonferroni correction. A p -value of less than 0.05 was considered a significant change. All the analyses were performed using SAS software (SAS Institute Inc., Cary, NC, USA, 2002–2012).

Data availability

The datasets analysed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This article was written in loving memory of Prof. Livio Corain, who passed away in April 2023. Livio conveyed to all of us his great passion for science combined with his enthusiasm and positivity in facing difficulties.

This research was funded by the University of Padova, Italy, grant number BIRD 210581. The funding body did not play any role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Open access funding provided by Università degli Studi di Padova.

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Authors and Affiliations

Department of Animal Medicine, Production and Health, University of Padua, Padova, Italy

Simona Neri, Barbara Contiero, Ilaria Iacopetti & Anna Perazzi

Department of Industrial Engineering, University of Padua, Padova, Italy

Maria Vittoria Mascolini, Silvia Todros, Emanuele Luigi Carniel & Chiara Giulia Fontanella

Centre for Mechanics of Biological Materials, University of Padua, Padova, Italy

Maria Vittoria Mascolini, Silvia Todros, Emanuele Luigi Carniel, Chiara Giulia Fontanella & Anna Perazzi

Department of Comparative Biomedicine and Food Science, University of Padua, Padova, Italy

Antonella Peruffo & Marco Patruno

RFX (CNR, ENEA, INFN), Padova, Italy

Matteo Zuin & Luigi Cordaro

CNR, Institute for Plasma Science and Technology, Padova, Italy

Department of Physics “G. Occhialini”, University of Milano – Bicocca, Milano, Italy

Emilio Martines

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Contributions

AP2 and CGF were responsible for the conception and design of the study. SN, AP1, MZ , LC and EM carried out corneal dissection and treatment, while MVM, ST and CGF carried out mechanical tests. CGF was responsible for data extraction and interpretation of the results, BC and MVM carried out the statistical analysis. AP2 acquired funding for the research project. CGF, SN and AP2 supervised the research activity. SN and MVM were mainly responsible for drafting the manuscript. ELC, MP, AP1, II and AP2 were involved in revising the draft. All authors reviewed the manuscript.

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Correspondence to Simona Neri or Antonella Peruffo .

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Ethical review and approval were waived for this study, because no live animal was sacrificed for this research. Experiments were performed on animal tissues collected at a local abattoir from carcasses of slaughtered animals destined to food market, in compliance with the Italian and European laws (Council Directive 93/119/EC, Council Regulation no. 1099/2009, Law no. 131/2013).

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Neri, S., Mascolini, M.V., Peruffo, A. et al. How does atmospheric pressure cold helium plasma affect the biomechanical behaviour on alkali-lesioned corneas?. BMC Vet Res 20 , 153 (2024). https://doi.org/10.1186/s12917-024-03980-6

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Received : 16 November 2023

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DOI : https://doi.org/10.1186/s12917-024-03980-6

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