research proposal on cervical cancer in ethiopia

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• Published: 18 September 2015

Willingness and acceptability of cervical cancer screening among women living with HIV/AIDS in Addis Ababa, Ethiopia: a cross sectional study

• Netsanet Belete 1 ,
• Yosief Tsige 2 &
• Habtamu Mellie 3  

Gynecologic Oncology Research and Practice volume  2 , Article number:  6 ( 2015 ) Cite this article

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In Ethiopia, cervical cancer (CC) ranks the 2nd most frequent cancer and the country had 27.19 million women at risk of developing the disease though only 0.6 % women age 18-69 years was screened every 3 years. Nearly a quarter (22.1 %) of southern Ethiopia HIV (Human Immunodeficiency Virus) infected Women were positive for precancerous cervical cancer. Doing regular screening can prevent the disease by around half (45 %) of the cases in age of 30s and three quarter (75 %) cases in 50s and 60s.In the presence of high risk for acquiring cervical cancer among HIV patients, willingness and acceptance of the screening is low in Addis Ababa, Ethiopia thus the current study was aimed to assess willingness and acceptability of cervical cancer screening and its determinants among women living with HIV/AIDS in Addis Ababa, Ethiopia.

A facility based cross sectional study was conducted among HIV positive women attending HIV treatment centers in Addis Ababa. The respondents were identified using systematic random sampling method. Data was collected using pretested questionnaire and were entered in to Epi-info version 3.5.1 software and exported in to SPSS version 20 statistical package for analysis. The criterias for entering independent variables into multivariate analysis were having p-value 0.05 or less at bivariate analysis and not co-linear.

One third (34.2 %) of participants knew cervical cancer and two third (62.7 %) were willing for the test though only a quarter (24.8 %) were accepted the test. The independent variables significantly associated with acceptance of screening were educational level, source of information, awareness for the test and preventability of the disease.

In current study willingness and acceptance of CC (cervical cancer) were low thus organizations working on cancer and HIV/AIDS should establish cervical cancer screening program and further enhance awareness creation.

In women, cervical cancer is the fourth most common cancer accounting about 20.4 % of all cancers globally, with an estimated 528,000 new cases in 2012 [ 1 , 2 ]. Majority (85 %) of the global burden occurs in the less developed regions, where it accounts for almost 12 % of all female cancers. In sub-Saharan Africa, 34.8 new cases of cervical cancer are diagnosed per 100, 000 women annually and it happens in about 60 % women living with HIV infection [ 3 – 5 ].

There were an estimated 266,000 global deaths from cervical cancer in 2012, accounting for 7.5 % of all female cancer deaths. Almost nine out of ten (87 %) CC deaths occur in less developed regions. In sub-Saharan Africa, the mortality is 22.5 per 100,000 though it is less than 2 per 100,000 in Western Asia, Western Europe and Australia/New Zealand [ 1 , 2 ].

In 2014, the expected diagnosis and death from invasive cervical cancer in America was 12,360 and 4,020 respectively [ 6 ].

More than one fifth of all new cervical cancer cases globally are diagnosed in India. In the country, the disease ranked 2nd cause of female cancer. According to 2012 estimate, the country annual diagnosed cases and deaths from the disease was 122,844 and 67,477 respectively [ 2 , 7 ]. In Taiwan the incidence rate of the disease among HIV infected women was 712.08/100,000 person-years [ 8 ].

In 2012, Ethiopia has a population of 27.19 million women aged 15 years and older who are at risk of developing cervical cancer. Current estimates indicate that every year 7095 women are diagnosed with cervical cancer and 4732 die from the disease. The disease ranks 2nd most frequent cancer among women. The disease has crude incidence rate of 16.3 per 100,000 populations per year in the country. Only 0.6 % women age 18–69 years was screened every 3 years [ 9 ].

As evidences showed HIV infected women are at risk for CC [ 10 – 13 ]. Cervical cancer is about 7.9 times more common in HIV infected women than none infected ones [ 10 ]. Cervical squamous intraepithelial lesion was about 7.04 times higher in HIV positive compared HIV negative women [ 12 ]. Nearly a quarter (22.1 %) of Southern Ethiopia HIV-Infected Women were positive for precancerous cervical cancer [ 13 ].

Cervical cancer which is caused by persistent infection with human papillomavirus [ 1 , 7 , 12 , 14 – 17 ] is preventable disease, yet the number of cases globally is expected to almost double by the year 2025 [ 18 ]. Doing regular screening (no more than once every three to five years) can prevent the disease by around 45 of the cases in age of 30s and 75 % cases in 50s and 60s [ 19 , 20 ]. Screening can be done using Pap smear [ 20 ], human papillomavirus testing [ 21 ] and visual inspection with acetic acid [ 22 ].

In the presence of high risk for acquiring cervical cancer among HIV patients, awareness and acceptance of the screening is low. In Boston, of eligible women for screening about 53.0 % had not undergone screening [ 23 ]. In Kenya teaching and referral hospital the self-reported screening uptake was 17.5 % [ 24 ]. About half (56.2 %) of HIV positive Nigerian women were aware of cervical cancer. In same country, only one every ten (9.4 %) of HIV positive women were screened for cervical cancer [ 25 ].

In Addis Ababa, Ethiopian women had very low awareness of cervical cancer and the etiology of cervical cancer was thought to be due to breaching social taboos or undertaking unacceptable behaviors. As a result, the perceived benefits of modern treatment were very low [ 26 ].

Although cervical cancer is a leading cause of cancer related morbidity and mortality among women in Ethiopia, its screening coverage as part of HIV care was low, only covers less than 1 % due to have no national screening program [ 18 , 27 , 28 ]. Hence the current study used to assess the willingness and acceptability of cervical cancer screening and its determinants among HIV positive women. The obtained information will be used for decision makers and organizations working on cancer and HIV/AIDS to consider and integrate cervical cancer screening as part of HIV/AIDS diagnosis and treatment guideline since there is no prior local evidence up to our knowledge.

Methods and materials

Study design and setting.

A cross-sectional study design using both quantitative and qualitative research method was conducted on HIV treatment centers in Addis Ababa which is the capital city of Ethiopia. In the town, there are 45 hospitals, 72 health centers, and 43 health posts owned by ministry of health [ 29 , 30 ]. These service sites were providing HIV diagnosis and treatment and its related supportive services. There are about 210,306 people living with HIV/AIDS in Addis Ababa of which 124,609 are women [ 31 ].

All HIV infected women above age of 17 years and coming for chronic HIV care in public health institutions of Addis Ababa during study period were the study populations.

Sample size determination and sampling strategy

The sample size for quantitative part was determined by a single population proportion formula using 95 % confidence interval (a = 0.05), 5 % margin of error (d) and the proportion (p) of cervical cancer screening in women living with HIV/AIDS from prior studies, which was 27.0 % [ 32 ].

The final sample size after adding 10 % contingency was 333.

For qualitative part two women from each referral hospital and one woman from each health centers was selected for in-depth interview.

Among Addis Ababa regional health bureau owned public health institutions, three referral hospitals and eight health centers providing ART service were selected for study by lottery method. To calculate the sampling interval for quantitative study, the HIV patient flow for the past six consecutive months before data collection period was taken from each selected health institutions and added for approximation of future sampling frame. Selection of participants was done using systematic random sampling method based on arrival order of HIV infected women to the health institution for medical care. The staring participant was selected by lottery method from sample interval. The interviewed participant’s corresponding medical record was reviewed for assessing laboratory measurements like CD4 count and clinical stages of HIV/AIDS.

For qualitative data, purposive sampling method was used to select women for the in-depth interview in selected health institutions. Women who were not selected for interview in quantitative study were included for qualitative part.

Data collection procedure and data quality management

For quantitative study, a structured questionnaire which was developed by reviewing different literatures was used for data collection. The questionnaire was translated in to local language (Amharic) and back translated to check consistency. The data collection tool was pretested among 16 patients and identified errors were corrected accordingly. The outcome variable of the study was cervical cancer screening acceptability. For the qualitative aspect a semi-structured interview guide was prepared in English and translated to local language of Amharic version. The in-depth interview was tape recorded and note was taken during interview.

To maintain quality of data; standardized and pre- tasted data collection tools were used for both quantitative and qualitative studies. Appropriate training was given for data collectors and supervisors. Daily supervision was carried out by supervisors and principal investigators to check completeness of the questionnaire. The quantitative data was entered twice by trained data clerk to check correct data entry. In addition at the end of data entry data cleaning were done using frequencies, cross tabulations, sorting and listing to check missed values and outliers. Errors identified during data collection were corrected accordingly at the field and those errors occurred during/after data entry were corrected by revising the original questionnaire.

Operational definitions

Willingness to be screened for cervical cancer - if a women willing for testing but not decided to be screened in the near future [ 25 ].

Acceptance to be screened for cervical cancer- if a women willing for testing and decided to be screened in the near future” [ 25 ].

Knowledgeable about cervical cancer- if participant answers 7 questions out of 13 Knowledge assessment questions.

Data analysis

For quantitative data, code was given and entered in to Epi-info version 3.5.1 software and exported in to SPSS version 20 statistical package for analysis. Multi-co-linearity was checked using Pearson correlation, tolerance or variance inflation factor and there were not multi-co-linearity. Independent Variables associated with outcome variable with p-value 0.05 or less at bivariate analysis and not co-linear were entered into multivariate analysis via binomial logistic regression to get adjusted predictors. Descriptive statics of continuous variables were presented using mean, median and discrete variables were presented using percentage, and tables. P -value <0.05 was used as cut off point of statistical significance for analytical analysis.

The qualitative in-depth interview was translated to English version by arranging the points according to forwarded questions. Then framework analysis method was employed to grasp the detail information.

Ethical issue

The study proposal was approved by the institutional review board of Addis Ababa University. Letter from the Research Ethics Committee was submitted to Addis Ababa regional health bureau to get permission for conducting the study. To protect anonymity and confidentiality of the participants, both data collectors and supervisors were working in ART clinics in addition personal identifier data was not collected. Informed written consent was obtained from respondents after explaining the purpose of the study.

A total of 322 study participants were included with a response rate of 96.7 % and about 14 in depth interviews were conducted based on saturation of information.

Characteristics of the study participants

The dominant ethnicity and religion were Amhara (53.7 %) and orthodox Christianity (71.7 %) respectively. Mean age of the study participants was 35.65 (SD ±10.17). Most of them were educated (78.3 %) and about half of them were have no regular source of income (51.2 %), had experience of pregnancy 1–2 times (47.5 %), diagnosed as having HIV before 6–10 Years ago (49.1 %). Most of (91.9 %) the participants were initiated ART and were WHO clinical stage 2 (34 %) HIV patients.

On card review, CD4 count of 211 (65.5 %) participants were less than or equal to 500 cells/ul, and the remaining 111(34.5 %) were CD4 count greater than 500 cells/ul. Most of the participants in the qualitative were attended secondary education, married and were between the age of 29 and 35.

Cervical cancer awareness, knowledge and test acceptance

Of the whole participants 110 (34.2 %) know about cervical cancer. And their major sources were health professionals during contact on routine HIV chronic care 59 (53.6 %), media 64 (58.2 %), reading books 13 (11.8 %), and friends 11(10.0 %) and the least was from family 3 (2.7 %). Regarding knowledge assessment only 81 (25.1 %) was found to be knowledgeable.

Even though they didn’t have detail knowledge regarding the disease, most of the in-depth participants were aware of cervical cancer. Some of the participants agree as it is the cancer of the female reproductive tract. Medias are mentioned as a source of knowledge about the disease for most of the participants and some of them also experience the disease in their family members and neighbors.

Majority of participants 97 (88.2 %) believe as the disease is a preventable. Similarly from the qualitative part, most of the participants believed as cervical cancer is a preventable disease. A young respondent mention that “one can get prevented from cervical cancer by having the screening test regularly”.

About one third 31.4 % (101) participants knowing the availability of the screening procedures for the disease and about one third (62.7 %) were willing to screened for cervical cancer and a quarter (24.8 %) of them were decided to screened in the near future.

Most of the participants repudiate to take the screening test due to assuming, the test is time consuming 43 (35.8 %) (Table  1 ). The mentioned reasons in in depth interview were high cost of the test and timing consuming, fear of result of the test (being diagnosed as having cervical cancer), and a recently HIV diagnosed woman noted that “the word you have a cancer diagnosis is really irritating beside my HIV, I think I will get hopeless, if I am diagnosed as having cervical cancer”.

Only 37 (11.5 %) of the study participants were ever tested for cervical cancer in their life time. The time of screening was before HIV/AIDS diagnosis (29.7 %), within one year of HIV/AIDS diagnosis (32.5 %) and after one year of HIV/AIDS diagnosis (37.8 %). Of those who get the screening test, about 11(29.7 %) were positive for the test.

In multiple logistic regression, after adjustment for potential cofounders, the factors that enhance accepting of screening were being in age group of 40–49, 50–59 and >60 years compared <29; having above 12 grade educational level compared to read and write; having regular source of income; getting information about cervical cancer from health professionals, having awareness of the test and needing the screening to take early measure. Respondents not knowing cervical cancer as preventable were less likely to accept the screening (Table  2 ).

In this study one third (34.2 %) participants knew the availability of screening test for CC and this finding was similar with HIV positive women in Lagos, Nigeria (34.5 %) [ 25 ] and it was higher than two studies in Nigeria (15.5 %) [ 33 ], (6.5 %.) [ 34 ]. The possible reasons for discrepancy of the result might be variation in study populations i.e. all women [ 33 , 34 ] vs HIV infected women in current study, regional state or country specific promotion policy variations, variations in involvement of the CC education in media and its exposure and differences in socio-cultural condition.

In current study majority of participants mentioned as health professionals were their main source of information for CC and the finding is in agreement with prior studies [ 33 , 35 – 37 ].

The current finding of two third participants (62.7 %) willing to be screened for cervical cancer were lower than a study done in Nigeria (96.5 %) [ 38 ] and Mozambique (84 %) [ 39 ] and the difference might be attributed by variations in health policy on promotion of CC, variations on awareness creation using mass-media and socio-economic variations.

The current study revealed as one every ten (11.5 %) participants were ever tested for CC in their life time and this is in line with a study in rural Mozambique (11 %) [ 39 ], Sokoto, Nigeria, (10 %) [ 40 ], two studies in Kenya (12.3 %) [ 41 ] and (17.5 %) [ 25 ] and HIV positive women in Lagos, Nigerian (9.4 %) [ 25 ]. The finding was higher than two studies in Ogun State, Nigeria (4.8 %) [ 34 ] and (9.5) [ 42 ] and it was lower than a study among HIV-positive women Ottawa, Ont (58 %) [ 23 ]. The reason of being higher than Ogun State, Nigeria [ 34 , 42 ] might be attributed by variations of study populations i.e. all women in [ 35 ] since HIV infected women may frequently visit health institutions and can get health professionals which are the main source of information for screening [ 33 , 35 – 37 ].

The current finding of most of the participants not willing to take the test due to assuming that the test is time consuming (35.8 %), fear of being positive for the test (30.8 %) and high cost of the test (30.0 %) was in agreement with the a similar study in HIV positive women in Lagos, Nigerian [ 25 ] and Kenya [ 41 ].

In this study, participants having above 12 th grade educational level compared to read and write, and having awareness about CC were 1.2 and 3.6 times respectively more likely accepting the screening and the finding was in parallel with a study among HIV positive women in Lagos, Nigerian in which having a tertiary education were enhancing screening by 1.4 times (OR = 1.4; 95 % CI: 1.03-1.84) and those aware of cervical cancer were 1.5 times (OR: 1.5; 95 % CI: 1.2-2.0) more likely accepting the screening [ 25 ].

In current study, participants who were getting information about cervical cancer from health professionals were 6 times more likely accepting the screening and this finding was supported by prior studies [ 33 , 40 ].

Conclusion and recommendation

One third (34.2 %) participants knew cervical cancer and two third (62.7 %) were willing for the test though only a quarter (24.8 %) were accepted the test. After adjustment in multivariate analysis, the factors that enhance accepting of screening were being in age group of 40–49, 50–59 and >60 years compared <29; having above 12 th grade educational level compared to read and write; having regular source of income; getting information about cervical cancer from health professionals, having awareness of the test, needing screening to take early measure and knowing cervical cancer as preventable disease. Thus organizations working on cancer and HIV/AIDS should further work to enhance awareness, and acceptability of the test. Ethiopian ministry of health should establish CC screening program since two third participants were willing for screening. Screening refusals as a result of assuming time consuming of the test, fear of the test result and anticipated high cost need to be addressed through advocacy and public mobilization. A further study with a large sample size is recommended to validate the current finding.

Abbreviations

Acquired immunodeficiency syndrome

Antiretroviral treatment

• Cervical cancer

Human Immunodeficiency Virus

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Acknowledgment

We would like to thank Addis Ababa University for its financial support. The authors thank the counselors at each institution and health providers working in each HIV treatment unit and study participants for their cooperation in the success of this work.

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Netsanet Belete

Addis Ababa University, Allied School of Health Science, Addis Ababa, Ethiopian

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Authors’ contributions

NB has brought the research idea, develops the proposal, coordinated the data collection and performed the statistical analysis. YT has participated in development of the proposal, coordinated the data collection and performed the statistical analysis. HM was participated in development of the proposal, coordinated the data collection and performed the statistical analysis and prepares the manuscript. All authors read and approved the final manuscript.

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Belete, N., Tsige, Y. & Mellie, H. Willingness and acceptability of cervical cancer screening among women living with HIV/AIDS in Addis Ababa, Ethiopia: a cross sectional study. gynaecol oncol res pract 2 , 6 (2015). https://doi.org/10.1186/s40661-015-0012-3

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DOI : https://doi.org/10.1186/s40661-015-0012-3

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Uptake of pre-cervical cancer screening and associated factors among reproductive age women in Debre Markos town, Northwest Ethiopia, 2017

• Simachew Animen Bante 1 ,
• Simegnew Asmer Getie 1 ,
• Almaz Aklilu Getu 1 ,
• Kebadnew Mulatu 2 &
• Selamawit Lake Fenta 1  

BMC Public Health volume  19 , Article number:  1102 ( 2019 ) Cite this article

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Cervical cancer remains a major cause of morbidity and mortality among women, particularly in low-resource countries like Ethiopia. Early screening for pre-cervical cancer is a key intervention in reduction of maternal deaths. We assessed uptake of pre-cervical cancer screening and its associated factors among women of reproductive age in Debre Markos town in northwest Ethiopia.

A community-based, cross-sectional study was conducted among 517 women of reproductive age. A multistage sampling technique was used to select study participants. Kebeles (sub-districts) were selected by a simple random sampling technique.Data was entered using Epi Info and analyzed by SPSS. Variables in binary logistic regression with a P value < 0.2 were fitted to multivariable logistic regression. Significant variables were declared at 95% CI and an AOR of P value < 0.05.

A total of 517 women were interviewed with100% response rate. Results revealed only 108 women (20.9%) [95% CI =17.6–24.6] had been screened for pre-cervical cancer. Participants ages 35–49 [AOR = 3.21, 95% CI: 1.40, 7.39] informed by health professionals about cervical cancer [AOR = 6.65, 95% CI: 3.64, 12.15], positive attitude to screening [AOR = 3.38, 95% CI: 1.92, 7.61], visited health institution once or more in a year [AOR = 6.72, 95% CI: 2.40, 18.79], visited health institution once or more in two years [AOR = 3.76, 95% CI = 1.39, 10.19], history of sexually transmitted infections [AOR = 2.37, 95% CI: 1.11, 5.07] and family history of cervical cancer [AOR = 4.95, 95%CI: 1.62,15.15] were significantly associated with pre-cervical cancer screening.

Uptake of pre-cervical cancer screening was found to be low among women of reproductive age. Age, attitude, informed by health provider, visiting health institution, history of sexually transmitted infections and family history of cervical cancer were found to be significantly associated with higher uptake of screening. To scale up currently limited uptake of pre-cervical cancer screening, community health education should be undertaken, leading to attitude change for young women.

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Cervical cancer is the second commonly diagnosed cancer and the leading cause of cancer death in African women [ 1 ]. The prevalence of cervical cancer is high in low- and middle-income countries due to lack of awareness for cervical cancer screening, higher rate of Human Papilloma Virus (HPV) infection and inaccessibility of screening [ 2 ].

Every year more than 270,000 women die worldwide from cervical cancer [ 3 ]. Cervical cancer is usually detected in advanced stages in developing countries due to lack of effective preventive mechanisms. An estimated 80%of all patients with cancer in developing countries are presented with advanced stages at their first visit [ 1 ].Poor access to screening and treatment services attributed to more than 85% of women’s death in low- and middle-income countries [ 4 ]. Death rates vary from country to country. This is due to lack of screening services for the prevention and early detection of the disease [ 1 ].

Even with the presence of these major problems, only few women receive pre-cervical cancer screening services in Ethiopia. Uptake remains low due to screening methods -only visual inspection with acetic acid (VIA) and because the test is not patient-friendly in terms of privacy [ 5 ].

For the past many years, high-income countries have seen a dramatic drop in cervical cancer incidence and mortality. However, similar success has not yet been achieved in low- and middle-income countries like Ethiopia. This is largely due to little information about pre-cervical cancer screening. In many countries, offering VIA to all young adolescent girls and preventive treatment programs has been radically increased. But much remains to be done, especially in the lower-income countries like Ethiopia where the burden of cervical cancer is highest [ 4 ].

Maternal morbidity and mortality related to cervical cancer is the second most occurring and the leading killer of women among all cancer types in Ethiopia. Studies have shown that uptake of pre-cervical cancer screening is very low, for example, in the towns of Arbaminch (5.9%) and Dessie (11%) [ 6 , 7 ] compared to the National cervical cancer prevention strategic plans (80%) set by Federal Ministry of Health of Ethiopia [ 8 ]. Additionally, the factors associated with low coverage have not been well investigated. Therefore, engagement in cervical cancer prevention and screening could result in one of the most significant successes to decrease women mortality and morbidity related to cervical cancer in Debre Markos town as well as in the country [ 5 ].

Most pre-cervical cancer screening studies in Ethiopia have been conducted on knowledge and attitude. Only a few studies were conducted on pre-cervical cancer screening practice and associated factors. Hence, there is limited evidence on the uptake of pre-cervical cancer screening(PCCS) and associated factors in most regions of Ethiopia [ 9 ]. This community-based study will play vital role in generating data that is important to fill gaps for program and policy makers. It can also be a source for advancing further study in the field of cervical cancer prevention.

Study setting, period and participants

A community based, cross-sectional study was conducted from March 01, 2017 to April 01, 2017 in Debre Markos town, capital of East Gojjam zone, northwestern Ethiopia. The town is located at 300 km far from Addis Ababa, capital of Ethiopia and 265 km from Bair Dar, capital of Amhara regional state. According to the 2015 Census, the town has a total population of 113,101, of which, 60,425 were women. There are seven kebeles , one referral hospital, three health centers and five nongovernmental clinics which are giving different reproductive health services in the town. It is only the government hospital that gives pre-cervical cancer screening service. All women in reproductive age group who are living in Debre Markos town were source populations. Therefore, all women in reproductive age group who were available during data collection period in selected kebeles were study populations. In this study, women who had been living in Debre Markos town for at least six months and age group from 15 to 49 years old were included. Women who were seriously ill and women who had total abdominal or vaginal hysterectomy were excluded.

Sample size and sampling procedure

The sample size was calculated by using the single population proportion formula with the assumption of 95% CI, and 11% proportion of women who had undergone pre- cervical cancer screening in Dessie town [ 10 ]. 10% non-response rate and 4% margin of error was used to obtain sample size of 235. Since the sampling technique was multistage, design effect of 2 was considered as well as with adjustment of 10% non- response rate, the final sample size was 517. Four Kebeles were selected by simple random sampling technique. The total sample size was proportionally allocated for each Kebele . Study subjects were selected by systematic sampling technique. Sampling fraction was determined by dividing the total households in each kebele for the sample size which was proportionally allocated in each kebele . The first household was selected by lottery method and then every 27th interval in each kebele was included in the study. Women within reproductive age group were interviewed from the selected households and if there were more than one woman in the household, lottery method was used to select one.

Data collection tools and techniques

The questionnaires were adapted from related study [ 11 ]. It was first prepared in English and then translated in Amharic (local language) and back translated into English by language experts to ensure uniformity. Interviewer administered pre-tested questionnaire was used for data collection. The data were collected by four diploma midwives and supervised by two BSc midwives. Data collectors and supervisors were trained for two days prior to data collection. Pre-test was done on 26 individuals other than selected kebeles . Personal identifiers were not included in the questionnaires to ensure participants confidentialities. The questionnaires were checked on daily bases by supervisors and principal investigator.

Variables and measurements

Independent variables in this study were classified into 5 sections: these were socio- demographic characteristics, reproductive characteristics, knowledge related variables, attitude related variables to pre-cervical cancer screening, visiting health facility and health providers related variables were used to assess the uptake of pre-cervical cancer screening in this study. The dependent variable in this study was ever being screened for pre-cervical cancer screening.

Twenty three questions were asked on knowledge of pre-cervical cancer screening: source of information about pre-cervical cancer screening, symptoms of cervical cancer, screening practice and causes of cervical cancer. The response to each of the questions was “yes” or “no”. The responses were scored and summed. Each response was given a score of one for correct answers and zero for incorrect once. The cut-offs were defined knowledgeable and not knowledgeable using median scores.

The attitude of the participants about pre-cervical cancer screening were early prevention, the burden of the cervical cancer, severity, susceptibility, barriers for screening, results of pre-cervical cancer screening and treatment were measured using Likert scale which ranges from score 4 (strongly agree) to score 1 (strongly disagree). The responses were summed up and a total score was obtained for each respondent. The median score was calculated and those who scored above median score of attitude assessing questions were categorized as having positive attitude about pre-cervical cancer screening and those who scored the median value or less than the median of attitude assessing questions were categorized as having negative attitude about pre-cervical cancer screening.

Reproductive age women

Women aged from 15 up to 49 years old [ 12 ].

Screening uptake

The proportion of women who have ever been screened for pre-cervical cancer at least once in life time [ 13 ].

Knowledgeable

Study participants who scored above the median score of 23 knowledge assessing questions [ 14 ].

Not knowledgeable

Study participants who scored the median value or less than the median score of 23 knowledge assessing questions [ 14 ].

Positive attitude

Study participants who scored above median score of 7 attitude assessing questions [ 14 ].

Negative attitude

Study participants who scored the median value or less than the median of 7 attitude assessing questions [ 14 ].

Data processing and analysis

Data entry and cleaning was done with Epi Info 7. Data were exported to SPSS version 21 for analysis. Descriptive statistics were analyzed and presented using tables and figures. The outcome variable is binary in its nature and it is labeled as “1” when the participants were screened for PCCS, otherwise “0”. Frequencies and proportions were computed for description in relation to socio-demographic and other variables. Strength of statistical associations was determined using adjusted odds ratio with 95% confidence interval. Relationships between each independent variable and outcome variable were investigated using binary logistic regression model. Those variables with P- value less than 0.2 at the bivariable level were included in a multivariable logistic regression model for controlling potential confounding effect. In the multivariable analysis, variables with p- value < 0.05 were considered as associated factors.

Socio-demographic characteristics

A total of 517 reproductive age group women interviewed making 100% response rate. The mean age of the participants was 30.1 years (SD ±7.9). Two hundred twenty eight (44.1%) of them were in the age group of 25–34 years (Table  1 ).

Reproductive characteristics

More than half of the participants 297 (57.4%) had single sexual partner. 443 (85.7%) of participants and most 511 (98.8%) had no history of STI and smoking respectively (Table  2 ).

Knowledge and attitude of participants about pre-cervical cancer screening

In this study, 240 (46.4%) of participants were knowledgeable about pre-cervical cancer screening. More than half 266 (51.5%) of participants did not hear about pre-cervical cancer screening. The dominant source of information was health professionals 110 (43.8%) followed by television 97 (38.6%) (Fig.  1 ).

Source of information for study participants regarding to pre-cervical cancer screening in Debre Markos town, northwestern Ethiopia, March– April2017 ( n  = 251)

Two hundred twenty-nine (44.3%) participants had positive attitude about pre-cervical cancer screening.

Uptake of pre-cervical cancer screening

In this study, uptake of pre-cervical cancer screening was 108 (20.9%). The reasons mentioned by participants for not being screened were being healthy (42.7%) followed by lack of information about PCCS (27.9%), (Fig.  2 ).

Main reasons not to be screened for pre-cervical cancer among who had never screened in Debre Markos town, northwestern Ethiopia, March – April2017 ( n  = 409)

Factors associated with uptake of pre-cervical cancer screening

In bivariable analysis; age, income, informed about cervical cancer by health professionals, knowledge of women on cervical cancer, given birth, number of partner, knew someone diagnosed with cervical cancer, attitude of women on cervical cancer, history of STI, family history of cervical cancer, and visiting health institution were statistically significant with the uptake of pre-cervical cancer screening.

Multivariable logistic regression showed age, informed about cervical cancer by health professionals, attitude of women on cervical cancer, family history of cervical cancer, history of STI and frequency of visiting health institutions were associated with uptake of pre-cervical cancer screening (Table  3 ).

This study found that those women who were in the age group of 35–49 years were 3.21 times more likely to take pre-cervical cancer screening than those whose ages were between 15 and 24 years [AOR = 3.21, 95% CI: 1.40, 7.39].

Those women who were informed by health professionals about cervical cancer were 6.65 times higher to take pre-cervical cancer screening as compared to those who were not informed [AOR = 6.65, 95% CI: 3.64, 12.15].

Women who had positive attitude about cervical cancer were 3.38 times more likely to take pre-cervical cancer screening than their counter parts [AOR = 3.38, 95% CI: 1.92, 7.61].

Participants who had visited health institutions once or more in a year were 6.72 times higher and those who had visited health institution once or more in two years were 3.76 times higher to be screened as compared to those who never visited [AOR = 6.72, 95% CI: 2.40, 18.79 and [AOR = 3.76, 95% CI: 1.39, 10.19] respectively.

Participants who had history of STI were 2.37 times more likely to take pre-cervical cancer screening than those who had no history of STI [AOR = 2.37, 95% CI: 1.11, 5.07].

Participants who had family history of cervical cancer were 4.95 times higher to use pre-cervical cancer screening when compared to those who had not [AOR = 4.95, 95% CI: 1.62,15.15].

The uptake of pre-cervical cancer screening among women of reproductive age was 20.9% (95% CI =17.6–24.6%), which is lower than the Federal Ministry of Health National cervical cancer prevention strategic plans (80%) [ 8 ].

The result is in line with studies done in Kenya (25%), Tanzania (21%) and in Ethiopia (19.8%) [ 11 , 15 , 16 ]. However, this finding was lower than the study conducted in Thailand (65.9%), Jamaica (66%) and in Kenya (39%) [ 17 , 18 , 19 ]. The reason may be due to accessibility of the service, having many methods of pre-cervical cancer screening and availability of more trained health providers. It may also be due to differences in socio-demographic characteristics such as the level of education of the study participants in the countries. Age of the study participants might also be another possible reason. The method of the study may also contribute to the difference. In a facility-based study as participants might get information from health providers, it increases the uptake of pre-cervical cancer screening. This finding was higher than the study conducted in Nigeria (8%) [ 20 ], Uganda (4.8%) [ 21 ], Dessie (11%) [ 10 ] and Arbaminch, Ethiopia (5.9%) [ 6 ]. This difference might be brought by age and other socio-demographic characteristics difference of study participants. The difference could also partially explain by the time gap between the studies as well as the study area might be different among the studies.

This study showed that maternal age was one of the significant predictors of pre-cervical cancer screening uptake. Women in the age group 35–49 were 3.21 times more likely to be screened as compared to mothers in the age group 15–24 (AOR = 3.21, 95% CI = 1.40–7.39). This finding is supported with previous studies conducted in Greece, Jamaica, Mekelle, Arbaminch and Dessie [ 6 ]. The possible explanation could be that cervical cancer symptoms usually develop in women above 30 year sold. Additional explanations may be that Ethiopian health policy encourages screening of more than 30 years old women. It may also be due to the fact that as age increases they may be multipara so they might visit health institution for antenatal care, post-natal care and for delivery, while at the same time receiving information about cervical cancer.

History of sexually transmitted infections was a significant factor for pre-cervical cancer screening uptake. Women who had a history of sexually transmitted disease were 2.37 times more likely to be screened as compared to those participants who had no history of sexually transmitted disease (AOR = 2.37, 95% CI =1.11–5.07). This study is in line with studies done in Kenya, Kasarani and Mekelle [ 11 , 22 ]. When women are treated for STIs at institutions, they could be told about the relationship of cervical cancer and STIs by the health provider so that they could get screened. These participants might also be near for reproductive health services so that they might further check other reproductive services like cervical cancer screening.

Family history of cervical cancer was other significant factor for uptake of pre-cervical cancer screening. Those participants who had history of cervical cancer in their family were 4.95 times more likely to be screened as compared to their counterparts (AOR = 4.95, 95% CI = 1.62–15.15). This is the first report and there are no other studies that support those participants who had family history of cervical cancer were more likely to screen pre-cervical cancer screening. The possible reason might be that women who had family history of cervical cancer would think that cervical cancer will be inherited genetically so that they would screen by fear of this.

Attitude of participants was significant predictor of pre-cervical cancer screening. Participants who had positive attitude were 3.38 more likely to be screened than those participants who had negative attitude (AOR = 3.38, 95% CI = 1.92–7.61). This finding is in line with studies conducted in Ilorin, Nigeria and Dessie, Ethiopia [ 20 , 23 ]. Anticipated reasons for this might be those participants who had positive attitude about cervical cancer could believe pre-cervical cancer screening will prevent from developing cervical cancer.

Visiting health institutions was also significant factor for pre-cervical cancer screening. Those participants who were visiting a health institution for any reason once or more in a year were 6.72 times higher (AOR = 6.72, 95% CI = 2.40, 18.79) and once or more in two year were 3.76 times higher (AOR = 3.76, 95% CI = 1.39, 10.19) to be screened as compared to those participants who never visited health institution. This finding is in agreement with previous studies done in Jamaica and Kenya [ 24 , 25 ]. The explanation might be that women who had visited health institution frequently would have higher chance of getting more comprehensive information from health professionals in the form of health education or counseling about pre-cervical cancer screening.

Getting information about cervical cancer from health providers was a significant predictor for uptake of pre-cervical cancer screening. Those participants who were informed by health providers about cervical cancer were 6.65 times higher to be screened as compared to their counter parts (AOR = 6.65, 95% CI = 3.64–12.15). This is in line with the studies done in Thailand, Portland Jamaica, Trelawney Jamaica, Uganda and Ethiopia [ 14 , 17 , 18 , 26 , 27 ]. This might be due to the fact that these women were more responsive to health providers who educate them about the disease and preventive measures. In addition, these discussions could be excellent opportunity to address negative attitudes about cervical cancer. Other explanation might be that women who were informed by health providers about cervical cancer could have high awareness and knowledge and they might be screened PCCS.

Limitations of the study

The limitations of this study include that information was self-reported by participants and there was no way of verifying the screening.

Recommendations

Federal Ministry of Health and Amhara Regional State Health Bureau should utilize mass media to influence the attitude of women towards cervical cancer and increase health-seeking behavior through health information dissemination. They should also encourage women to have annual health checkups as well as change a program that helps to include all reproductive age groups as target groups.

Zonal and Woreda Health Offices should strengthen information distribution about pre-cervical cancer screening by health providers throughout the community in places such as schools, markets and colleges to aid in changing the attitude of women to be receptive to pre-cervical cancer screening and promote youth-friendly service areas to appeal to young women.

Health institution and health professionals should strengthen the diagnosis and treatment of STIs for all women of reproductive age as a means to increase pre-cervical cancer screening indirectly and give PCCS information to all reproductive women that come for any purpose to any facilities.

Further studies should be conducted among reproductive women in rural areas about pre-cervical cancer screening, including a qualitative study to explore why there is a limited screening utilization.

Conclusions

Pre-cervical cancer screening uptake was found to be low: Age group 35–49, informed by health professionals about cervical cancer, positive attitude to pre-cervical cancer screening, visited health institution, history of STI and family history of cervical cancer were a significant predictor for pre-cervical cancer screening uptake.

Availability of data and materials

The data sets generated during the study are available from the corresponding author upon request.

Abbreviations

Adjusted Odd Ratio

Cervical Cancer

Crude Odd Ratio

Ethiopian Birr

Health Facility

Human Immunodeficiency Virus

Health Provider

Human Papilloma Virus

Oral Contraceptives Pills

Precancerous Cervical Lesion

Pre- Cervical Cancer Screening

Standard Deviation

Statistical Package for Social Sciences

Sub Saharan Africa

Sexually Transmitted Infections

Visual Inspection with Acetic acid

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Acknowledgements

We would like to acknowledge Bahir Dar University, College of Medicine and Health Sciences, Department of Midwifery. Our sincere and deepest gratitude goes to Debre Markos town administration. We would also like to extend our thanks to data collectors, supervisors and study participants.

This work was funded by Bahir Dar University for data collection. The funder had no role in study design, data analysis, and interpretations of data or writing of manuscript.

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Simachew Animen Bante, Simegnew Asmer Getie, Almaz Aklilu Getu & Selamawit Lake Fenta

Department of Public Health, College of Medicine and Health Sciences, Bahir Dar University, Bahir Dar, Ethiopia

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SAB wrote the proposal, led study design, analyzed the data, drafted the manuscript and ensured that all authors approved the manuscript before submission. SAG approved the design and reviewed the manuscript. AAG revised subsequent drafts of the paper and reviewing the manuscript. KMM involved in data analysis and reviewed of the manuscript. SLF approved the proposal and reviewed the manuscript.

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Ethical approval was obtained from the Institutional Review Board of College of Medicine and Health Science, Bahir Dar University. Letter of permission was obtained from Amhara National Regional Bureau and Debre Markos town administration office. Both written and verbal consent was obtained from study participants after the purpose of the study was explained. Written consent was received from adult next-of-kin when the respondent was less than 18 years of age and verbal assent was obtained from less than 18 years age of participants. Participants were informed that participation was voluntary and they could withdraw at any time. Personal identifiers were not included in the questionnaires to ensure participant confidentiality.

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Bante, S.A., Getie, S.A., Getu, A.A. et al. Uptake of pre-cervical cancer screening and associated factors among reproductive age women in Debre Markos town, Northwest Ethiopia, 2017. BMC Public Health 19 , 1102 (2019). https://doi.org/10.1186/s12889-019-7398-5

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Research Article

Utilization of cervical cancer screening and associated factors among women in Debremarkos town, Amhara region, Northwest Ethiopia: Community based cross-sectional study

Roles Conceptualization, Data curation, Formal analysis, Methodology, Writing – original draft

* E-mail: [email protected]

Affiliation Department of Midwifery, Debremarkos University, Debremarkos, Ethiopia

Roles Methodology, Supervision, Writing – review & editing

Affiliation Department of Midwifery, University of Gondar, Gondar, Ethiopia

Roles Formal analysis, Supervision, Writing – review & editing

• Bewket Yeserah Aynalem, 
• Kiber Temesgen Anteneh, 
• Mihretu Molla Enyew

• Published: April 7, 2020
• https://doi.org/10.1371/journal.pone.0231307
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Introduction

Cervical cancer is the most common type of malignancy among all malignancies for women worldwide with 266 000 deaths every year. Even though there is a proven importance of cervical cancer screening, the death of women due to cervical cancer in Ethiopia is high. We, therefore, did this study to investigate the utilization of cancer screening and its associated factors among women in Debremarkos town, Amhara region, Ethiopia.

A community-based cross-sectional study was conducted among women from 30–49 years in Debremarkos town, from July 1 to August 30, 2018. A multistage sampling procedure was used to select 822 women in the study. We used EPI info version 7 for data entry and SPSS version 24 software for cleaning and analysis. Bivariable and multivariable logistic regression analyses were performed to identify factors associated with the utilization of cervical cancer screening. Variables with a p-value of less than 0.05 were taken as significant variables.

The study revealed that 44 (5.4%) of women have been screened for cervical cancer. Women’s age [AOR:3.126(1.246,7.845)], marital status (AOR:3.41(1.299,8.972)], educational status(secondary education level [AOR: 4.578(95% CI: 1.19, 17.65)] and College and above education level [AOR:7.27,95%CI: 2.07,25.513)]), started sexual intercourse for the first time below 16 years[AOR:3.021(1.84,4.97)], history of multiple sexual partners [AOR:2.51(1.040, 6.06)], history of sexually transmitted disease [AOR:4.04(1.68, 9.72),], knowledge on cervical cancer screening [AOR:4.02(2.07,7.77)] and attitude towards cervical cancer screening [AOR:3.23(2.52,4.12)] were significant factors for utilization of cervical cancer screening

This study showed the magnitude of the utilization of cervical cancer screening is very low. Women’s age, marital status, educational status, age at first sex history of multiple sexual partners and sexually transmitted disease, knowledge and attitude were important factors of screening. Therefore, intervention programs that are aimed at improving cervical cancer screening practice among women should focus on the identified factors.

Citation: Aynalem BY, Anteneh KT, Enyew MM (2020) Utilization of cervical cancer screening and associated factors among women in Debremarkos town, Amhara region, Northwest Ethiopia: Community based cross-sectional study. PLoS ONE 15(4): e0231307. https://doi.org/10.1371/journal.pone.0231307

Editor: Nülüfer Erbil, Ordu University, TURKEY

Received: June 11, 2019; Accepted: March 20, 2020; Published: April 7, 2020

Copyright: © 2020 Aynalem et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Cervical cancer is the most common malignancy among all malignancies for women worldwide [ 1 ]. In 2012, about 266, 000 deaths occurred due to cervical cancer worldwide and 90% of cases occurred in Low and Middle-Income Countries (LMICs); the highest was occurred in Sub Saharan Africa (SSA) where cervical cancer is the leading killer among women[ 2 ]. In Ethiopia,7095 cases and 4732 death of cervical cancer occur every year [ 3 ].

Cervical cancer screening has been proven to be a very effective prevention strategy for cervical cancer [ 1 , 4 , 5 ]. The United States Preventive Services Task Force (USPSTF), the American Cancer Society (ACS) World Health Organization (WHO) guidelines state screening for cervical cancer once within lifetime reduces significantly the risk of mortality from cervical cancer and incidence of advanced cervical cancer [ 6 – 8 ]. The WHO recommended age for cervical cancer screening should be limited to women the age of 30 to 50 years since there is evidence on younger age women with a milder degree of lesion spontaneously recover to normal [ 5 , 9 , 10 ].

Ethiopia adopted the WHO guideline and advised women to start cervical cancer screening at age of 30–49 years at least one to three years interval with the approach of seeing and treat through Visual Inspection under Acetic acid (VIA) as screening strategy and cryo-therapy as a treatment method[ 1 , 4 , 5 , 11 ].

Despite the importance of screening, a high incidence of cervical cancer is still a big problem and a major cause of morbidity and mortality of women in LMICs especially in SSA [ 12 , 13 ] and the lowest cervical cancer screening rate found in Ethiopia which accounts below 1% [ 14 ].

Therefore, the main aim of this research was to identify factors affecting cervical screening utilization and recommend ways to increase screening utilization by the community.

Study area and period

This study was conducted in Debremarkos town, Amhara region, Northwest Ethiopia from July 1 to August 30, 2018. Debremarkos town is the capital city of East Gojjam Zone that is found in the Amhara region, North West Ethiopia, which is located at 300 km from Addis Ababa, the capital city of Ethiopia and 265 km from Bihar Dar, the capital city of Amhara region. There are one referral hospital, three health centers and five non-governmental clinics that give different reproductive health services in the town. Only the government referral hospital gives cervical cancer screening services.

Study design

A community-based cross-sectional study design was employed.

Study participants

The source population was all women age 30–49 years old who were residents of Debremarkos town. The study population was women age 30–49 years old who were residents of Debremarkos town during the study period in the selected kebeles. We excluded women who are not permanent residents of the town (less than six months) and those who were critically ill during the data collection period.

Sample size

The sample size for prevalence was determined based on a single population proportion formula assumption. The expected proportion of cervical cancer utilization (19.8%) from the previous study in Ethiopia at Mekelle town[ 15 ]and a 3.5%confidence limit (margin of error) was used.

With considering design effect 1.5 since it had two stages and the sample size was calculated as498*1.5 = 747then the non-response rate was also considered to be 10%and 747*0.10 = 75.Then the final sample size was747+75 = 822.

Sampling techniques

A multistage sampling technique was used and firstly all the kebeles found in the Debremarkos town were listed in a frame. Then three out of the seven kebeles were selected by the lottery method. Again the list of households found and coded in each kebele. The size of households consisting of eligible population to be selected from each kebele was determined proportionally based on the size of the study units and the k th value was computed for each selected kebele. The woman of the selected household was interviewed and if there was more than one woman in the household, the lottery method has been used to select only one. In the case of absenteeism, after three repeated visits the next eligible woman was included in the study.

Study variables

Dependent variable..

Utilization of cervical cancer screening

Independent variables.

Socio-Demographic Characteristics, Reproductive and behavioral characteristics, and knowledge and attitude on cervical cancer and its screening.

Operational definitions

Utilization of cervical cancer screening..

Refers to the proportion of persons eligible to be screened within a population who have been screened within 3 years for cervical cancer[ 15 ].

Multiple sexual partners.

Those women who have ever had penetrative sexual intercourse with more than one partner in their life serially or at the same time [ 16 ].

Cigarette smoking.

The active smoking or ever had a smoking history of women one or more manufactured or hand-rolled tobacco cigarettes per day which excludes passive smokers [ 17 ].

Knowledgeable.

Women who answered knowledge questions score of mean value or above were considered as knowledgeable.

Favorable attitude.

Women who answered attitude questions a score of mean value or above were considered to have a favorable attitude.

Data collection and data quality control

To assure the data quality, data were collected with face to face interviews by three trained BSc Midwives after one-day data collection training was given to them together with three MSc holder supervisors. The questionnaire was structured and pre-tested which was first prepared in English and translated to local (Amharic) language and then again translated back to English. A pretest was conducted on 42 women of the sample size in other than the study area and the necessary correction on the tool was employed accordingly.

Data processing and analysis

Epi Info version 7 software was used for data entry and SPSS version 24 for used for analysis. Bivariate logistic regression was employed to identify an association between independent and dependent variables. Variables having a P-value of less than 0.2 in the bivariate logistic regression analysis were fitted into the multivariable logistic regression model. The 95% confidence interval of odds ratio was computed and variable having P-value less than 0.05 in the multivariable logistic regression analysis was considered as statistically significant.

Ethical clearance

Ethical clearance was obtained from the Ethical Review Committee of the Department of Midwifery, under the delegation of the institutional review board of the University of Gondar. Ethical clearance and formal letters were also obtained from the University Gondar School of Midwifery and were submitted to Debremarkos health office and permission was obtained. Finally, written informed consent was also obtained from each study participant.

Socio-demographic characteristics of the respondents

All 822 study participants responded to the questionnaire, giving a response rate of 100%. The mean age of the study participants was 36.81 years (36.81 ±5.14 SD). The majorities of women were Amhara 809 (98.4%), Christian religion 789 (96%) and married 768(64.8%). Two hundred thirty-one (28.1%) of the women have not attended formal education ( Table 1 ).

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Reproductive and behavioral characteristics

Two hundred one (24.5%) study participants first had sexual intercourse at age 16 and below. Women who had a history of multiple sexual partners (MSPs) within three years were 461 (56.1%). And 129 (15.7%) had a history of sexually transmitted disease (STD). Six hundred eighty-nine (83.8%) of the study participants had used modern family planning method at least for one year. Six hundred sixty-three (80.7%) got birth at least once. Around ninety-seven (11.8%) of respondents had a family history of cervical cancer and 17 (2.1%) of the respondents had also smoking history ( Table 2 ).

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Knowledge, attitude and utilization of cervical cancer screening

More than half of the respondents (59%) were knowledgeable about cervical cancer screening ( Table 3 ). More than half of the respondents (57.4%) had a favorable attitude towards cervical cancer screening ( Table 4 ). Forty-four (5.4%) of the study population have been utilized cervical cancer screenings a minimum of once within the last three years with [95% CI: 3.8, 7.1]( Table 5 ).

https://doi.org/10.1371/journal.pone.0231307.t003

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Factors associated with utilization of cervical cancer screening

After controlling the effect of other variables with binary logistic regression, age, marital status, educational status, age start at first sexual intercourse, history of MSP, history of STD, duration of FP use, family history of CC, gravidity, knowledge, and attitude about CC screening continued to be significantly associated with utilization of cervical cancer screening (P-values<0.2).

After controlling the effect of other variables with multivariable logistic regression analysis, women’s age [AOR: 3.126 (95% CI: 1.246, 7.845)], marital status [AOR: 3.41 (95% CI: 1.299, 8.972)], education level (secondary education level [AOR: 4.578(95% CI: 1.19, 17.65)] and College and above education level [AOR:7.27,95%CI: 2.07,25.513)]), age started sexual intercourse for the first time [AOR:3.021(95%CI:1.84, 4.97)], history of MSP[AOR:2.51 (95% CI:1.040, 6.06)], history of sexually transmitted disease [AOR:4.04(95% CI:1.68, 9.72)], knowledge about cervical cancer screening [AOR:4.02,95% CI:2.07, 7.77)] and attitude about cervical cancer screening [AOR:3.23,95%CI;2.52, 4.12)] were significant factors for utilization of cervical cancer screening ( Table 6 ).

https://doi.org/10.1371/journal.pone.0231307.t006

This study was conducted to assess the cervical screening practice among women in Debremarkos town, northwest Ethiopia. Accordingly, the study found that only 5.4% of women had cervical cancer screening practice. Similarly, factors like women’s age, marital status, education level, and age at first sexual intercourse below 16 years old, history of STDs, knowledge, and attitude towards cervical cancer screening were significantly associated with utilization of cervical cancer screening.

The study finding of cervical cancer screening utilization (5.4%) in the current study was in-line with similar reports in Arbaminch town, Southern Ethiopia(5.9%)[ 18 ]. The finding of this research was lower than the studies done at Addis Ababa, Ethiopia(10.8%) [ 19 ], at Mekelle town, Northern Ethiopia(19.8%) [ 15 ], at Hadiya Zone, South Ethiopia (9.9%)[ 20 ], in Ethiopia (17%) [ 21 ], Kenya(16%)[ 22 ]and Nigeria (11%) [ 23 ].The possible explanation for this might be the difference in the age of study population; the difference in the study area; the difference in the health status of the study population; the difference with sample size; the difference with the level of knowledge and attitude of the study population.

The finding of this study was also higher than studies done in Ethiopia (2.9%) [ 17 ] and Southern Ghana (0.8%) [ 24 ]. The possible explanation might be the difference in the study area and study population; the difference in the age of the study population.

As shown in this study, women’s age was one of the significant factors for the utilization of cervical cancer screening. Women in their age 40–49 years were 3.126 times more likely to utilize cervical cancer screening as compared to women in their age of 30–39 years [AOR:3.126(95% CI:1.246, 7.845)]. This finding was supported by the studies done in Northern Ethiopia, Addis Ababa, Southern Ethiopia, Ethiopia and Malawi [ 15 , 17 , 18 , 25 , 26 ]. The possible explanation for this might be like women's age increases the probability of getting information about cervical cancer and its screening will be increased which leads them utilized cervical cancer screening service. The other explanation also might be increasing risk with women’s age leads the women to have more contact health facilities.

Marital status was also one of the significant predictors for the utilization of cervical cancer screening. This study showed that women who were single/divorced/widowed 3.414 times more likely utilized cervical cancer screening as compared with married women [AOR:3.414,(95%CI:1.299,8.972)]. This result was supported by the study done in Thailand [ 27 ]. The possible explanation for this might be single women are more likely educated since they might be young and divorced women or widowed women are a more likely aged and increasing risk with women's age leads the women to have more interest to visit health facilities.

Educational status was also the main significant factor for the utilization of cervical cancer screening. Women who took college & above education 7.268 times more likely utilized as compared with women who did not take formal education [AOR: 7.268(95% CI:2.071,25.513)].Similarly, Women who attended secondary education 4.578 times more likely utilized as compared with women who did not attend formal education [AOR: 4.578 (95% CI: 1.187,17.649)]. This study was supported by the study done in Ethiopia and Kenya [ 17 , 22 ]. This might be explained with, as the level of education increases, the women will have the chance to know about cervical cancer and its screening.

Age at first sexual intercourse was a significant predictor for the utilization of cervical cancer screening. Women who had started sexual intercourse with their age of 16 years and below were 3.021 times more likely to utilize cervical cancer screening as compared to those women who had started sexual intercourse after their age of 16 years[AOR: 3.021 (95%CI; 1.84, 4.97)]. The possible explanation for this might be women who started sexual intercourse at an early age, may have increased lifetime sexual partners which in turn increase the chance of being infected with sexually transmitted infection (STI) and STD with its signs and symptoms which lead to visit health facilities. No literature found to compare with this study because it is sensitive to issue information biases might occur which was tried to avoid these biases in our study with care full interviewing technique.

This study finding showed that woman who had a history of MSPs was another important factor for utilization of cervical cancer screening. Women who have had a history of MSPs were 2.51 times more likely to utilize cervical cancer screening as compared to those who did not MSP [AOR: 2.51(95% CI: 1.040, 6.062)]. This study was supported by the result of a study done in Addis Ababa, at Mekelle, Malawi, and Thailand [ 15 , 25 – 27 ]. The possible explanation might be women, who had MSP history, would have the chance to be infected with STIs with its signs and symptoms which increases health facility visits.

The current study result showed that a woman who had a history of STD was another important factor in the utilization of cervical cancer screening. Women who have had a history of STD were 4.037 times more likely to utilize cervical cancer screening as compared to those who did not have STD history [AOR: 4.037, (95%Cl: 1.68, 9.72)]. This result was supported by the finding from Addis Ababa and Northern Ethiopia [ 15 , 25 ]. The above association might be explained by women who have STDs and history of STD, will have an increased chance of visiting health institutions for treatment and other medical help.

Women’s knowledge about cervical cancer screening was another significant factor in the utilization of cervical cancer screening services. Women who were knowledgeable about cervical cancer screening were 4.02 times more likely to utilize cervical cancer screening service as compared to those who were not knowledgeable [AOR:4.02 (95% CI:2.07, 7.77)]. This finding was supported by the result of studies done in Northern Ethiopia, Malawi, Tanzania, and Thailand [ 15 , 26 – 28 ]. The above reports might be explained by increasing the level of women’s knowledge about the benefits of screening directly lead the women to utilize cervical cancer screening.

Similarly, women’s attitude about cervical cancer screening was also a significant factor for utilization of cervical cancer screening service. Women who had a favorable attitude about cervical cancer screening were 3.225 times more likely to utilize cervical cancer screening service as compared to those who had unfavorable attitudes [AOR:3.225 (95%CI:2.52, 4.12)]. This study was supported by a study done in Northern Ethiopia, Southern Ethiopia, Southern Ghana and Thailand [ 15 , 18 , 24 , 27 ]. The above reports might be explained with women who have a favorable attitude towards cervical cancer screening will have self-initiative to know about cervical cancer risk factors and benefits of its screening.

This study showed the magnitude of the utilization of cervical cancer screening was lowin Debremarkos town, Northwest Ethiopia. Age of the women, marital status, and educational status, age at first sexual intercourse, history of multiple sexual partners and sexually transmitted disease, knowledge and attitude were statistically significant factors of the utilization of cervical cancer screening.

Acknowledgments

We would like to thank the University of Gondar and Debremarkos health office for their permission to this research and we gratefully acknowledge all study individuals for their participation in the study.

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Cervical cancer in Ethiopia – predictors of advanced stage and prolonged time to diagnosis

• Matthias Begoihn 1 ,
• Assefa Mathewos 2 ,
• Abreha Aynalem 2 ,
• Tigeneh Wondemagegnehu 2 ,
• Ulrike Moelle 1 ,
• Muluken Gizaw 3 , 4 ,
• Andreas Wienke 3 ,
• Christoph Thomssen 1 ,
• Dawit Worku 5 ,
• Adamu Addissie 3 , 4 ,
• Ahmedin Jemal 6 &
• Eva Johanna Kantelhardt   ORCID: orcid.org/0000-0001-7935-719X 1 , 3  

Infectious Agents and Cancer volume  14 , Article number:  36 ( 2019 ) Cite this article

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Introduction

In Ethiopia, most cervical cancer patients present at advanced cancer stages, long time after they experience first symptoms. We investigated possible predictors of long time spans between symptom onset and pathologic diagnosis (patient intervals). We also aimed to seek out predictors for advanced cancer stage diagnosis.

We conducted a retrospective cohort study among 1575 cervical cancer patients who were registered at Tikur Anbessa Specialized Hospital (TASH), Addis Ababa, Ethiopia between September 2008 and September 2012. Cox proportional hazards regression was used to find predictors of long patient intervals. Cumulative odds ordinal logistic regression was used to identify predictors of cancer stage at diagnosis.

Median patient interval was 30 weeks, with the interval substantially longer in patients residing in rural than urban areas. Longer patient intervals were associated with more advanced cancer stages at pathologic diagnosis. HIV-positive women had an almost 1.5 times increased risk of diagnosis at a more advanced stage.

Cervical cancer patients are diagnosed after long time periods leading to advanced stages at diagnosis. Measures to raise awareness about cervical cancer, to increase screening and to shorten the time interval from recognition of symptoms to diagnosis are urgently needed.

Cervical cancer incidence and mortality has been drastically reduced in high resource countries during the last decades. This can be largely attributed to the implementation of screening programs for the detection of precancerous lesions and HPV and improved therapy [ 1 , 2 ]. Yet in low- and middle income countries where access to such measures is limited, cervical cancer remains a significant health problem. The vast majority of an estimated number of 311.000 cervical cancer deaths worldwide occur in less developed regions [ 3 ]. In Ethiopia, where almost 6.300 new cases are diagnosed annually, about 4.884 women die from cervical cancer each year. This makes cervical cancer the second-most common cancer in the country, and the second-most deadly cancer among Ethiopian women [ 4 ].

One of the most important prognostic factors is stage at diagnosis, linking early-stage diagnosis with better chances of survival [ 5 ]; still most cervical cancer patients present at advanced stages in Ethiopia [ 6 ]. Studies examining predictors of late and advanced stage presentation of cervical cancer patients in low- and middle-income countries have been scarce [ 7 ]. The relationship between HIV-infection and cervical cancer and the question of whether HIV-infection leads to more advanced cancer stages is discussed controversially [ 8 , 9 , 10 ]. The timespan between symptom onset and diagnosis has been associated with stage at diagnosis [ 11 ], but other studies could not confirm this [ 12 , 13 ]. However, these studies were conducted in high-income countries where time to diagnosis is considerably shorter. It is unclear whether these results likewise apply to low-income countries such as Ethiopia, where time to diagnosis is long and patients present at advanced stages. Tragically, in a previous study of a hospital cohort of 1.059 cervical cancer patients receiving oncologic treatment in Addis Ababa, Ethiopia, we found long periods of time between diagnosis and the beginning of cancer treatment. This led to stage-migration and thus decreased chances of survival [ 6 ].

In this study, using the same cohort (with the addition of patients who were diagnosed with cervical cancer but never received therapy) we focused on the time between patient reported onset of symptoms and pathological diagnosis (patient interval). The aim of this study was to find predictors for cancer stage at pathological diagnosis and longer patient intervals in Ethiopia. We further hypothesized that longer patient intervals lead to more advanced stages at diagnosis.

We conducted a retrospective cohort study among cervical cancer patients who registered at Tikur Anbessa Specialized Hospital (TASH), Addis Ababa, Ethiopia between September 2008 and September 2012 as described earlier [ 6 , 14 , 15 ]. TASH is the largest hospital in Ethiopia and the only hospital in the country currently offering radiotherapy – thus, people from all parts of the country were referred there for therapy. Early tumor stages from FIGO Ia - IIa were treated with radical hysterectomy with curative intentions. More advanced tumor stages and cases of unclear surgical margins were treated with external beam radiotherapy. At the time of the study, brachytherapy as recommended according to international guidelines was not available in Ethiopia.

Study population

Ethiopian woman who presented at TASH between September 2008 until September 2012 with a primary diagnosis of invasive cervical cancer were eligible for this study. Of 1655 collected patient files, we used 1575 cases for further analysis. Of these 80 patients were excluded: 42 patients presenting with recurrent disease; two asymptomatic patients who were incidentally diagnosed with cervical cancer; 35 with missing dates regarding pathological diagnosis or symptom onset; one with noninvasive cancer. Since there was no nationwide cervical cancer screening program in place, all women included presented with symptomatic disease. Information regarding patient characteristics, clinical characteristics such as histology, FIGO-Stage, symptoms and waiting times were retrieved from patient files from the oncology and gynecology ward.

Predictor variables

The patients’ residency was classified as urban or rural. Patients living in one of the 10 largest cities in Ethiopia were classified as ‘urban’, while the remaining patients living in smaller cities and villages were classified as ‘rural’. HIV-status was subdivided into two groups: positive HIV-status, and negative or unknown HIV-status. Comprehensive HIV-screening at TASH was routinely introduced after September 2011; before this time, only clinically-suspicious patients or patients with a high risk profile (e.g. those with an HIV-positive partner) were screened for HIV. The predictor variables in both models were preselected using variables that were coherent with similar studies [ 16 , 17 , 18 ]. Other risk factors commonly examined in regards to both late and advanced stage presentation include socioeconomic status variables such as low education and illiteracy [ 16 , 17 , 18 , 19 , 20 , 21 , 22 ]. These were not recorded in the patient files at TASH, and thus could not be assessed in this analysis.

Tumors were staged according to guidelines set by the International Federation of Gynecology and Obstetrics (FIGO) [ 23 ]. Stage at primary diagnosis when first seen by a physician was used for further analysis in this study. FIGO-stages were assessed around the date of pathology report. In most cases, a chest X-Ray and abdominal ultrasound followed. If there was an upstaging within 4 weeks after the first staging due to distant metastasis findings or hydronephrosis, the higher FIGO-stage was used. FIGO-stages were later grouped for statistical analysis into stage of FIGO I - IIa (patients receiving primary surgery), FIGO IIb, FIGO III (FIGO IIIa and IIIb) and stage of FIGO IV (IVa and IVb).

Time intervals

Patient interval was defined as the time interval between the date the patient noticed the first symptom and the date of the biopsy report. This interval was used because the date of the first symptom and the date of pathologic diagnosis were widely available, whereas the date of first presentation – i.e. when the patient was first seen by a clinician – was not documented for most patients. Data on symptom onset were abstracted from handwritten documents in the patient files. Patient interval was used as a continuous variable in weeks to avoid loss of power and bias [ 24 , 25 ].

Statistical analysis

Data were analyzed using SPSS Version 23. A cumulative odds ordinal logistic regression with proportional odds was conducted to examine the effect of time to diagnosis, HIV-status, place of residence and age on stage at diagnosis. The proportional odds assumption was assessed by a full likelihood ratio test. Odds ratios are presented with their corresponding 95% confidence intervals.

Cox proportional hazards regression was used to evaluate the association between predictors and the patient interval and to calculate hazard ratios (HRs) with 95% confidence intervals. Simple regression analysis was conducted using the predictor variables age, place of residence and HIV-status. For multiple regression analysis, we included all three variables into the model.

Patient characteristics

Mean age was 49 years (SD ±11.6 years). Known HIV-seropositive women presented at a mean age of 39 years, while patients with a negative or unknown HIV-status presented at a mean age of 50 years. One hundred thirty-five of the patients were tested HIV-seropositive (8.6%). Out of the 494 women screened for HIV, 135 women were screened positive and 359 were screened negative. The rest of the women where not screened. Of the HIV-seropositive women, 86.3% were on antiretroviral medication. Close to two thirds of the women came from rural areas. Most woman presented with advanced stages (55.2% stage IIIb or higher). Only 12.1% presented with an early FIGO-stage of I-IIa, making them eligible for surgery (Table 1 ).

Predictors for longer patient interval

Median patient interval was 30 weeks (range 0–526 weeks). It was shorter for HIV-positive women (25 weeks) compared to women with a negative or unknown HIV-status (30 weeks). Rural women received their pathologic diagnosis after a median time of 32 weeks whereas women from one of the 10 largest cities in Ethiopia were diagnosed after a median time interval of 25 weeks.

Univariate analysis indicated a higher risk for longer patient intervals for women from rural areas compared with woman coming from one of the 10 largest cities (HR 1.23; CI 1.11–1.36) (Table  2 ). Also more likely to be diagnosed later in univariate analysis were younger patients (HR 0.99) and women with a negative or unknown HIV-status (HR 1.19, (CI 1.004–1.43)). After entering all three variables (age, place of residence, HIV-status) in the multiple Cox-Model, the adjusted Hazard Ratio for HIV-status was 1.1 (CI 0.91–1.32) and for age 0.99 (CI 0.99–1). The adjusted Hazard Ratio for place of residence remained 1.23 (CI 1.11–1.36).

Predictors for more advanced stage at diagnosis

We found longer patient intervals associated with more advanced FIGO-stages at diagnosis in the proportional odds model (OR 1.004 (CI 1.002–1.006) p: < 0.001) (Table  3 ). This means that the odds of being diagnosed in a more advanced stage group increased by 0,004 every week. Patient interval was shortest for early stages (24 weeks for FIGO I-IIa) and longest for advanced stages (35 weeks for FIGO IV) (Fig.  1 ).

Box-plot showing median patient interval (time between symptom onset and pathologic diagnosis in weeks) with 25th and 75th percentile by FIGO stage group

Known HIV-infection was associated with an almost 1.5-fold risk of diagnosis at a more advanced stage compared to those patients with a negative or unknown HIV-status (95% CI 1.05–2.1 p  = 0.025). Our data suggested no association between place of residence, age and stage at diagnosis.

Symptoms at diagnosis

All patients presented with symptoms related to cervical cancer, with the most common symptoms being abnormal vaginal bleeding, abdominal pain and vaginal discharge (Table 4 ). Even in early stages I-IIa, 91.1% of patients presented with abnormal vaginal bleeding. Constipation was suggestive of late stage disease: 64% of the patients presenting with constipation were staged IIIb and higher.

We found that longer patient intervals increased the risk of advanced stage cervical cancer diagnosis. Previous studies on the effect of longer patient intervals on outcomes like advanced stage and impaired survival presented conflicting results. Consistent with our findings, in the 1980s Fruchter et al. reported an increased risk for presentation at advanced stages of cervical cancer after long patient intervals [ 11 ]. In contrast, Tokuda et al. in Japan found no association between patient interval and stage of cervical cancer in the 1990s. However, Japan is a high-resource country and median patient interval was only 30 days [ 12 ], differing substantially from the long patient intervals observed in Ethiopia.

We also found that HIV-infection was associated with more advanced cancer stages at time of diagnosis compared to patients with a negative or unknown HIV-status. The association of HIV and HPV is well-known, and previous studies repeatedly linked HIV-infection with a higher prevalence, incidence and persistence of HPV-infection and its progression into precancerous lesions (especially for patients with low CD4 cell counts) [ 26 , 27 ]. However, the association between HIV and invasive cervical cancer is less clear. Published data indicate a 1.6 to 2.4 increased risk of developing invasive cervical cancer for HIV-positive women [ 28 , 29 ]. The effect of seroprevalence of HIV on cancer stage at time of diagnosis in comparable settings is similarly hard to establish.

In South-Africa, Lomalisa et al. found that HIV-positive patients with a CD4 count of below 200/mm3 had significantly more advanced tumor stages than HIV-negative women [ 9 ]. Fruchter et al. found HIV-positive patients to be at elevated risk for advanced cervical cancer diagnoses in univariate analysis. That said, their observed study group was small and statistical significance ceased after adjusting their model for other variables [ 8 ]. Moodley et al. found advanced stages among both HIV-positive and -negative patients with no association between HIV-status and stage [ 10 ]. On average HIV-seropositive women in our study presented 11 years younger than patients with a negative or unknown HIV-status [ 14 ]; this is consistent with the previous scientific literature where HIV-positive women presented 10–15 years earlier than HIV-negative women [ 10 , 30 ]. The association of HIV-infection and advanced stage presentation of cervical cancer could potentially be explained by the HIV-associated immunodeficiency leading to a more rapid cancer growth, although other authors attribute this to molecular interactions between HIV and HPV [ 31 , 32 , 33 ]. Ibrahim et al. in Sudan identified high age and rural residence as predictors for advanced stage presentation [ 16 ]. Findings from similar studies in Morocco and South India include socioeconomic factors such as low education and illiteracy [ 17 , 19 ].

In our study, women from rural areas tended to have longer patient intervals. This may be attributable to a low awareness of cervical cancer and its associated symptoms or the lack of health facilities and skilled personnel in rural parts of the country. Macleod et al. reported a lack of awareness and a misinterpretation of the seriousness of symptoms as the main risk factor for long patient intervals [ 20 ]. Fear of finding cancer and socioeconomic factors like illiteracy were other common themes among comparable studies [ 11 , 17 , 21 ].

In multivariate analysis, rural origin was associated but both age and HIV-status were not associated with long patient intervals in our study. Other factors that presumably influence the length of the patient interval include financial and logistic factors including delays in health care service.

We observed long time periods of median 25 to 35 weeks between women noticing the first symptom and pathological diagnosis among all stages, increasing with FIGO-stage. A comparable study in Nepal found shorter patient intervals of median 22 weeks [ 18 ]. Even in early stages, women were often diagnosed after many weeks or months of experiencing symptoms of cervical cancer such as abnormal vaginal bleeding, pain and vaginal discharge. After pathological diagnosis, patients often had to wait months until radiotherapy started, which further increased the risk of cancer progression [ 6 ].

The key strength of this study is the large sample size with patients coming from all over Ethiopia. There are, however, certain limitations we need to acknowledge. Data regarding patient and tumor characteristics and dates used for the calculation of patient interval were extracted from handwritten medical records. These dates relied on self-reporting from patients who might have been subjected to recall bias. We do not know how well women remembered the date of symptom onset and how meticulously it was documented. Secondly, women who were symptomatic for a long time but never presented to a health care professional may have died at advanced stages without ever being diagnosed at TASH and thus did not appear in our study. Hence, such a selection bias might falsely result in favorable data, particularly for patients with advanced cancer stages. Since the date of first presentation to a health care professional was not available for many patients, it was not possible to identify precisely at which stages of the diagnostic pathway these delays occur. Some patients may have been clinically diagnosed earlier and then had to wait until referral for pathological diagnosis – yet for the patients for whom all data were available, this interval did not vary substantially between tumor stages and residence. Qualitative research is needed to identify the impediments to diagnosis which lead to long patient intervals and more advanced stage presentation.

Previous studies found that efforts in down-staging helped to significantly increase overall survival. A three-year program in rural Tanzania with the aim of down-staging cancer through proactive visits from trained health aides into people’s homes showed favorable results [ 34 ]. One study conducted in rural India found that a cervical cancer education group effectively reduced the ratio of advanced stage diagnoses and increased the number of women diagnosed at early tumor stages [ 35 ]. However, awareness of cervical cancer and knowledge of risk factors, signs and symptoms are still low among women in Ethiopia and other African countries [ 36 , 37 , 38 ]. In Malaysia, advanced cervical cancer presentation (stages III and IV) dropped from 60 to 26% within 4 years after a program was introduced, focusing on training health staff and strengthening public awareness through the use of pamphlets and posters in clinics and hospitals [ 39 ].

Prevention and down-staging programs could be integrated in HIV/AIDS care programs and other preexisting healthcare infrastructures like it has been successfully implemented in Zambia [ 40 , 41 ]. Alongside an increased coverage of HPV vaccination and screening, such initiatives could help reduce cervical cancer mortality and incidence worldwide.

Our results support the hypothesis that long patient intervals lead to more advanced cervical cancer stages at pathologic diagnosis. Especially rural women tended to be diagnosed late and need to be addressed through awareness programs. HIV-postive women were at elevated risk of advanced tumor presentation; this should encourage efforts of the government to implement specific screening programs for HIV positive women. In addition to the current government efforts to implement nationwide screening programs, information about signs and symptoms of the disease should be spread.

Availability of data and materials

The datasets analyzed are available from the corresponding author on reasonable request.

Abbreviations

Confidence Intervals

International Federation of Gynecology and Obstetrics

Human Immunodeficiency Virus

Human Papilloma Virus

Hazard Ratio

Tikur Anbessa Specialized Hospital

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Acknowledgements

Authors would like to thank the staff members of Tikur Anbessa Specialized Hospital Radiotherapy Center who treated and provided care for all cervical cancer patients. We also greatful to Mrs. Tinsae and Mrs. Tigist for obtaining the follow-up data and Mrs. Mulu and Mr. Neme for collecting the patient files.

This study was supported by the Federal Ministry of Research and Education of.

Germany, grant 01DG12006.

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Matthias Begoihn, Ulrike Moelle, Christoph Thomssen & Eva Johanna Kantelhardt

Radiotherapy Center, School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia

Assefa Mathewos, Abreha Aynalem & Tigeneh Wondemagegnehu

Institute of Medical Epidemiology, Biostatistics and Informatics, Martin-Luther-University, Halle (Saale), Germany

Muluken Gizaw, Andreas Wienke, Adamu Addissie & Eva Johanna Kantelhardt

Department of Preventive Medicine School of Public Health, Addis Ababa University, Addis Ababa, Ethiopia

Muluken Gizaw & Adamu Addissie

Department of Gynecology, School of Medicine Addis Ababa University, Addis Ababa, Ethiopia

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MB performed statistical analysis and drafted the manuscript. EK, AJ, MG, UM and AW participated in designing the study, analysis, reviewing and editing the final manuscript and contributed to the discussion. UM and MB collected the data at TASH in Addis Ababa, Ethiopia. All the authors were involved in drafting of the manuscript and read and approved the final form of the manuscript.

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Correspondence to Eva Johanna Kantelhardt .

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Begoihn, M., Mathewos, A., Aynalem, A. et al. Cervical cancer in Ethiopia – predictors of advanced stage and prolonged time to diagnosis. Infect Agents Cancer 14 , 36 (2019). https://doi.org/10.1186/s13027-019-0255-4

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DOI : https://doi.org/10.1186/s13027-019-0255-4

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• Cervical cancer
• Sub-Saharan Africa
• Patient interval

Infectious Agents and Cancer

ISSN: 1750-9378

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Cervical cancer in Ethiopia: survival of 1,059 patients who received oncologic therapy

Affiliations.

• 1 Department of Gynaecology and Institute of Clinical Epidemiology, Martin Luther University, Halle an der Saale, Germany; School of Public Health, Departments of Pathology and Gynaecology, and Radiotherapy Center, School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia; Department of Epidemiology, School of Public Health, Boston University, Boston, Massachusetts, USA [email protected].
• 2 Department of Gynaecology and Institute of Clinical Epidemiology, Martin Luther University, Halle an der Saale, Germany; School of Public Health, Departments of Pathology and Gynaecology, and Radiotherapy Center, School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia; Department of Epidemiology, School of Public Health, Boston University, Boston, Massachusetts, USA.
• PMID: 24951611
• PMCID: PMC4077439
• DOI: 10.1634/theoncologist.2013-0326

Background: Almost 500,000 women are newly diagnosed with cervical cancer (CC) every year, the majority from developing countries. There is little information on the survival of these patients. Our primary objective was to evaluate consecutive CC patients presenting over 4 years at the only radiotherapy center in Ethiopia.

Methods: All patients with CC from September 2008 to September 2012 who received radiotherapy and/or surgery were included (without brachytherapy). Vital status was obtained through telephone contact or patient cards.

Results: Of 2,300 CC patients, 1,059 patients with standardized treatment were included. At the end of the study, 249 patients had died; surviving patients had a median follow-up of 16.5 months; the 10% and 90% percentiles were 3.0 and 32.7 months, respectively. Mean age was 49 years (21-91 years). The majority of patients presented with International Federation of Gynecology and Obstetrics stage IIb-IIIa (46.7%). Because of progression during the waiting time (median 3.8 months), this proportion declined to 19.3% at the beginning of radiotherapy. The 1- and 2-year overall survival probabilities were 90.4% and 73.6%. If assuming a worst-case scenario (i.e., if all patients not available for follow-up after 6 months had died), the 2-year survival probability would be 45.4%.

Conclusion: This study gives a thorough 4-year overview of treated patients with CC in Ethiopia. Given the limited treatment availability, a relatively high proportion of patients survived 2 years. More prevention and early detection at all levels of the health care system are needed. Increasing the capacity for external-beam radiation as well as options for brachytherapy would facilitate treatment with curative intention.

Keywords: Africa; Ethiopia; Prognosis; Survival; Uterine cervical neoplasms.

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• Uterine Cervical Neoplasms / mortality*
• Uterine Cervical Neoplasms / pathology
• Uterine Cervical Neoplasms / therapy*

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The trend of change in cervical tumor size and time to death of hospitalized patients in northwestern Ethiopia during 2018–2022: Retrospective study design

Aragaw e. aguade.

1 Statistics Department, Under Natural and Computational Science College, University of Gondar, Gondar Ethiopia

Chalachew Gashu

2 Statistics Department, Under Natural and Computational Science College, University of Odabultum, Ethiopia

Tigist Jegnaw

Associated data.

The authors confirm that the data supporting the findings of this study are not publicly available because the data were used for an another analysis. However, data are available from the corresponding author on reasonable requests. The guarantor has full access to all the data in this study and takes complete responsibility for the integrity of the data and the accuracy of the data analysis.

Background and Aims

Cervical cancer is the fourth most common cause of cancer‐related death in the world. The objective of this study was to determine factors that affect the longitudinal change of tumor size and the time to death of outpat

A retrospective follow‐up study was carried out among 322 randomly selected patients with cervical cancer at the University of Gondar Referral Hospital from May 15, 2018 to May 15, 2022. Data were extracted from the patient's chart from all patients' data records. Kaplan–Meier estimator, log‐rank test, the Cox proportional‐hazard model, and the joint model for the two response variables simultaneously were used.

Among 322 outpatients with cervical cancer, 148 (46%) of them were human immunodeficiency virus (HIV) positive and 107 (33.3%) of them died. The results of joint and separate models show that there is an association between survival and the longitudinal data in the analysis; it indicates that there is a dependency between longitudinal terms of cervical tumor size and time‐to‐death events. A unit centimeter square rise in tumor size, corresponding to an exp(0.8502) = 2.34 times, significantly raised the mortality risk.

The study showed that HIV, stage of cancer, treatment, weight, history of abortion, oral contraceptive use, smoking status, and visit time were statistically significant factors for the two outcomes jointly.

Implications

As a result, adequate health services and adequate resource allocations are critical for cervical cancer control and prevention programs. Therefore, the government should provide adequate funding and well‐trained health professionals to hospitals to sustain screening programs with appropriate coverage of cervical cancer patient treatments.

1. INTRODUCTION

Cervical cancer is the fourth most common cancer among women worldwide, with an estimated incidence of 570,000 cases and 311,000 deaths, as reported in 2018. 1  This study aims to assess the epidemiology and risk factors in developing cervical cancer. An estimated 85% of deaths from cervical cancer worldwide occur in middle‐ and low‐income countries, which have mortality rates 18 times higher than that in developed countries. Cervical cancer is known to be caused by oncogenic subtypes of the human papillomavirus (HPV). The risk factors for developing cervical cancer include: sex with multiple partners, sexual activity at an early age, having many children, use of birth control pills, smoking, low socioeconomic status, sexually transmitted diseases, oral contraceptive use, and immune disorders. Epidemiological studies have shown that the risk of developing cervical cancer and contracting genital HPV infection is influenced by a variety of factors. Thus, cervical cancer is due to a variety of additional factors working together with cancer‐associated strains of HPV. 1

The cervical cancer epidemic in Africa is profound and complex with noninfectious and infectious risk factors and etiologic components. The cervical cancer epidemic in Africa is considered by the dual burden of noncommunicable and communicable disease, 2 health service preventive delivery challenges, 3 , 4 , 5 shortages of human resources for health, 6 access to treatment shortages, and low cervical cancer consciousness among the health providers and population. 7 , 8

Many research findings show that the HPV vaccine is effective in both preventing genital warts and cervical lesions in those patients who are vaccinated; the result found that patients who are vaccinated for HPV have a lower risk of developing cervical cancer than those patients who are not vaccinated. 9 , 10 , 11 , 12 However, the Centers for Disease Control and Prevention does not recommend HPV vaccinations for people older than 26, individuals aged between 27 and 45, and who are not effectively vaccinated due to a risk for new HPV infection. 13

Screening for cervical cancer is still essential due to the inefficient HPV vaccine protection offered. HPV vaccination protects only 70% of women against cervical cancer. 15 Techniques of screening include: visual inspection with acetic acid (VIA) with HPV testing and Pap smear for risk of HPV types. Some of these methods, such as rapid HPV DNA and VIA testing, are preferred in developing nations due to their ease and cost of manufacture. 16 Due to the lack of comprehensive cervical cancer treatments, early diagnosis and screening could reduce related mortality and morbidity. 17

Artificial intelligence (AI) provides an automated diagnosis that significantly resolves the screening issue, which is verified. 18 In recent years, AI has been used to diagnose a growing number of diseases, particularly in skin malignancies, 19 imaging tumors, 20 classification and detection of retinal diseases, 21 and gynecologic cancer. 22  AI can use sophisticated algorithms for image classification and recognition, process data autonomously, and extract features. 23 , 24 , 25 , 26

In 2020, there were 342,000 cervical cancer deaths; approximately 90% of these deaths occurred in low‐ and middle‐income countries. 26  Programs that enable girls to receive vaccines against HPV infection and women to receive frequent screenings and appropriate care are in place in high‐income nations. Screening makes it possible to find precancerous lesions at an early stage when they are still treatable. In low‐ and middle‐income countries, cervical cancer is frequently detected only after it has progressed and symptoms appear, as access to these prophylactic practices is limited. Additionally, access to cancer treatments (e.g., cancer surgery, radiation, and chemotherapy) can be restricted, which could have an adverse impact on the condition. 27

A total of 120,000 new instances of cervical cancer are diagnosed each year in Africa, accounting for 20% of all new cervical cancer diagnoses worldwide. Women in Africa make up a sizable portion of those who lack access to treatment and care for cervical cancer. The conventional surgical treatment for early cervical cancer, a radical hysterectomy, is not performed in many clinics and in many nations due to a lack of experience. The same is true of several African nations, with some having no radiation equipment at all. Nevertheless, some facilities are particularly well‐suited for clinical trial enrollment because they offer a higher level of care, see a lot of patients, and do so frequently. HPV and HIV prevention and screening, suitable imaging examinations, and access to adequate treatment (surgery, chemotherapy, and other forms of radiation therapy) are some of the issues faced in sub‐Saharan Africa when treating cervical cancer. 28 Regarding total national mortality in Ethiopia, cancer accounts for roughly 5.8% of the total, except for Addis Ababa, where population‐based data is available; it is thought that there are about 60,960 new instances of cancer diagnosed each year.

In Ethiopia, cervical cancer screening (CCS) guidelines advocate a “screen‐and‐treat” method, in which women aged between 30 and 49 years are screened and treated with cryotherapy. The guidelines suggested annual screening for women who were HIV positive and three times annual screening for other women, but the screening was not consistent and was usually determined by the availability of resources. 29

Women and their families are affected by cervical cancer anywhere in the world, but notably in places with few resources for screening, prevention and treatment. Cervical cancer affected 604,237 women worldwide in 2020, accounting for 6.5% of all female cancer cases.

In 36 low‐ and middle‐income nations, mostly in sub‐Saharan Africa, cervical cancer affects women more frequently than any other type of cancer. In 2020, cervical cancer is predicted to claim the lives of 341,843 women, 90% of whom live in underdeveloped nations with severely restricted access to services for prevention, screening, and treatment. Today, cervical cancer claims the lives of women more than childbirth does. 30 , 31  Ethiopia recorded 4884 deaths and 6294 new cases of cervical cancer in 2018, one of the utmost rates in the world. 1

The investigator observed, from the University of Gondar Referral Hospital (UGRH), that the number of patients with cervical cancer being admitted to the UGRH has been rising year over year. Every year, related to cervical cancer, there are several cases of women who are dead or lost to follow‐up. This suggests that there are factors influencing both the survival status of cervical cancer patients discharged from the hospital and the progression of cancers. This calls for a change in healthcare priorities and the most recent information on the development and associated difficulties of cervical cancer in Ethiopia. Therefore, it is crucial to evaluate the variables that influence the longitudinal evolution of tumor size and the time to event (death) of outpatients with cervical cancer. Furthermore, it appears from studies that less than 10% of women in Ethiopia had CCS. 10 , 11 , 32

The facts about Ethiopia mentioned above indicate that many women are at high risk for cervical cancer. While some studies have been done on cervical cancer, the majority of those done in Ethiopia concern knowledge, screening practices, and factors that predict how long cervical cancer patients will live after diagnosis. These studies range from 2008 to 2012. 10 , 33

The tumor size of outpatients with cervical cancer, which is one of the key factors affecting prognosis, was not highlighted in the study. In addition to this, they did not show covariates that are measured longitudinally and related to the event, and the association between the longitudinal change of tumor size and the time‐to‐event (death) outcome.

Studying the change in cervical tumor size and the mortality rates of outpatients with cervical cancer is crucial for all of the aforementioned reasons. To the best of the researcher's knowledge, no published work has recorded a joint model analysis of changes in tumor size and the time to event (death) among outpatients with cervical cancer. So, in the case of the UGRH, this study attempted to pinpoint the variables that influence the longitudinal change in cervical tumor size and the time to event (death) of outpatients with cervical cancer.

The major objective of this study was to determine the effects of the size of tumor and time to event of outpatients with cervical cancer at the UGRH; the specific objectives are as follows:

• ❖ To investigate factors influencing the time to event of outpatients with cervical cancer at the UGRH.
• ❖ To identify risk factors that affect tumor size of outpatients with cervical cancer at the UGRH.
• ❖ To examine the relationship between tumor size and time to event of outpatients with cervical cancer at the UGRH.

Any concerned legal body can use the output of the research to allocate proper human and material resources for cervical cancer healthcare institutions. On the other hand, healthcare institutions could provide fast and effective services for those women with high‐risk factors for cervical cancer.

This study raises awareness and education among individuals, society, the government, and any legal body about the risk factors for cervical cancer and their life expectancy. Researchers who intend to conduct research on the relationship between factors of tumor size and the time to event of women with cervical cancer might use the output of this research.

2. MATERIALS AND METHODS

2.1. study area.

The study area was the UGRH, which is located 720 km northwest of Ethiopia's capital city of Addis Ababa. The hospital has 500 beds available. The referral hospital provides for more than seven million populations in the catchment area. It provides subspecialty and specialty services, including internal medicine, surgery, pediatrics, gynecology and obstetrics, ophthalmology, psychiatry, and so on, in its outpatient and inpatient clinics. Based on registered data, there are more than 10,000 delivery services for mothers annually. 34

The target population of this research was all cervical cancer patients who were hospitalized between May 15, 2018 and May 15, 2022 and who met all the inclusion criteria included in this study. Patients who began cervical cancer therapy at the UGRH from May 15, 2018 to May 15, 2022 and who had at least two follow‐up visits to the department clinic for prescription refills were included in this study. Data regarding the repeated measurement of tumor size and time to death were extracted from the outpatient's chart, which contains clinical information and sociodemographics on all outpatients with cervical cancer who were followed up. In this study, outpatients with cervical cancer represent the number of patients who transfer from the hospital to another hospital or who either leave the hospital by any means or who follow the clinical treatment up to the discharge date or die before completing the treatment for any accident other than cervical cancer or those who are on treatment.

2.3. Methods

There are two main components of a joint model: the longitudinal outcome and the survival (time to event) outcome. The longitudinal component of the outcome variable measures the tumor size every 6 months. It is measured in centimeters squared, so it is a continuous variable that specifies a linear mixed model with random effects. The survival outcome measures the time to (event) death of outpatients with cervical cancer (0 = censored and 1 = event).

The Ethical Clearance Approval Letter was obtained from the Ethical Approval Committee, Department of Natural Computational Sciences, University of Gondar. An approval letter with a copy of the research proposal was submitted to the Department of Oncology, Gondar University Referral Hospital. Informed verbal consent was given due to the unavailability of cervical cancer outpatients at the GURH during data collection. Both institutions approved the use of informed verbal consent obtained by telephone from study participants. For deceased study participants, oral consent was obtained using the telephone number of the caregiver on the patient's chart. For those who consented to participate in the study, a retrospective review of patient charts from May 15, 2018 to May 15, 2022 provided information on outpatient sociodemographics, medical history, and treatment received.

The longitudinal submodel of the joint model was described both by the conventional linear mixed‐effects model assuming homogeneous within‐subject variance and by incorporating subject‐specific variance. Longitudinal data sets consisted of an outcome variable, y ij , and a px 1 vector covariate, x 1 i , observed at times t  = 1, 2, 3, …, n i , for subject i  = 1, 2, 3, …; the subject‐specific variance was used to assess whether individuals with different tumor size variabilities have different influence on time to event (death) of outpatients with cervical cancer

where μ i ( t ) = β 1 T X 1 i ( t ) is the mean tumor size,   w 1 i ( t ) = z i T ( t ) b i is a subject‐specific random effect, ε i ∼ N ( 0 , σ 2 ) is a sequence of mutually independent measurement error, and  w 1 i ( t ) is the true individual level tumor size after the overall mean trajectory and other fixed effects have been adjusted. The b i is a vector of random effects corresponding to the random effect explanatory variables z T ( t ) and modeled as IID N(0, Σ) random variables. With repeated observations, however, the correlation among values for a given subject must be taken into account. Longitudinal modeling between specific subject variations was performed to understand differences among individuals; the continuous model inside subjects' variations was employed to analyze changes over time. 35 , 36

The timing of an event is examined using a survival model that accounts for the time to occurrence and the censor and/or truncation. The hazard function is widely used to express the risk of an event at time t  and obtain from the probability that the individual gets the event at time t , assuming that he or she survive at that time. Kaplan–Meier (KM) estimator is a nonparameter estimator of survival analysis, which is used to describe the survival of patients both graphically and numerically.

The joint model consists of two linked submodels, the measurement model for the longitudinal process and the time‐to‐event model for the survival process. The joint modeling approach was used to obtain less bias and more efficient estimates. The association between longitudinal process and survival process may arise in two ways. One is through the use of common independent factors, and the other is through stochastic dependency between w 1 i and w 2 i .

Estimation for joint models is based on the maximization of the log‐likelihood corresponding to the joint distribution of the time‐to‐event T and longitudinal outcomes y , L ( T i , δ i , y i ∣ b i , θ ) , can be specified as

where θ = θ t T , θ y T , θ b T T denotes the full parameter vector, with  θ t denoting the parameters for the event time, θ y the parameters for the longitudinal outcome, and θ b the parameters for the random effect. Assume that given the observed history, the censoring mechanism and the visiting process are independent of the true event times and future longitudinal process.

The joint density for the longitudinal response together with random effect, p ( y i ∣ b i , θ ) p ( b i , θ )  , is given by

where qb denotes the dimensionality of random effects' vector and ∥ x ∥ = ∑ x i 2 1 / 2 denotes the Euclidian vector norm. Maximization of the log‐likelihood function l ( θ ) = ∑ i log ⁡ p ( T i , δ i , y i , θ ) with respect to θ can be achieved using the expectation maximization algorithm or Newton–Raphson algorithm. Missing values are a frequent problem in many real‐world data settings. Multiple imputations are the most common imputation technique for addressing missing values; this paper used multiple imputations to properly account for the uncertainty in the imputed values due to missingness. 37

It is required to compare many models using various methods to choose the parsimonious model that best fits the provided data. This paper used Akaike's information criterion, Bayesian information criterion, and likelihood ratio test. 38

The precise nature of the joint model was selected by comparing via standard error, association parameter ( α ), and confidence interval. The association parameters quantify the magnitude of the association between the longitudinal process and the event process. It indicates that there is a dependency between longitudinal terms of cervical tumor size and time‐to‐death events. For a better understanding, we used standardized residual plots, and the hypothesis test was a two‐sided test. The data were entered and cleaned using SPSS version 20, and they were analyzed using R statistical software version 4.1.3.

3.1. Descriptive analysis

In this study, we used the guidelines for reporting statistics for clinical research in urology 39 for the proper reporting, analysis, and interpretations of clinical research.

The change in tumor size among outpatients with cervical cancer, which was measured roughly every 6 months at the initial entry and again at the 6‐, 12‐, 18‐, 24‐, 30‐, 36‐, and 42‐month visits, is known as the longitudinal response. The sample sizes at eight time points are 322, 322, 297, 253, 208, 157, 114, and 85. Following up on patients allowed us to observe the sharply rising degree of incomplete information throughout time as a result of recovery, deaths, dropouts, missed clinic appointments, and transfers to other hospitals. The average change in tumor size was 26.16 cm 2 , with a standard deviation of 4.58 cm 2 .

The survival endpoint of interest in this study was death. Censored outpatients are those outpatients who missed contact due to lost follow‐up or transferring to another hospital. Hence, the time to death or death time in months was created by subtracting the date of first entry from the date of the last visit (death date). Thus, based on the data obtained from the UGRH, among 322 patients, 118 (36.6%) of them died, while the rest 204 (63.4%) were censored outpatients (Table  1 ).

Descriptive results of categorical variables of outpatients' cervical cancer.

Abbreviation: HIV, human immunodeficiency virus.

3.2. Log‐rank test and KM estimates

The KM curve for the smoking status of cervical cancer patients shows that patients who do not smoke have a higher chance of surviving than patients who smoke. The survival probability of outpatients who do not take oral contraceptives is greater than that of outpatients who do, according to the plot of the KM curve for oral contraceptive use. Plots of the KM estimates for the two selected categorical covariates: oral contraceptives and smoking status are displayed in Table  2  and the remaining categorical variables are presented in Figure  1 .

Log‐rank test of categorical independent variables.

Kaplan–Meier (KM) plot of oral contraceptive use and smoking status of patients, 2018–2022.

To assess the significance of differences across various factors, log‐rank tests were performed on all categorical variables. According to the null hypothesis, there is no discernible difference between the rates of survival for various categories of categorical variables. The log‐rank tests in Table  2 revealed that, at the 5% level of significance, there is no difference between groups of residence and education in terms of the time to death. Death rates among the study groups differ significantly for other categorical factors.

Table  3 indicates that the proportional‐hazard (PH) assumption states that the hazard ratios are constant across time. Therefore, the risk of failure must remain consistent regardless of how long patients have been observed. This hypothesis was tested using Schonfeld's residual and a GLOBAL test. To test the assumption of the Cox proportional hazard (PH) model, we first fitted a univariable Cox PH model. The univariable Cox PH regression models are fitted for each covariate to find factors affecting patients' survival from cervical cancer before moving on to more complex models. The problem with the single covariate approach is that it ignores the potential that a collection of variables, each of which has only a very weak relationship to the outcome, can come together to significantly predict the outcome.

Cox proportional‐hazard assumption of outpatients with cervical cancer.

Based on the univariable results, the building blocks for a multivariable Cox model are as follows: baseline weight of patients; smoking status; histology type; HIV, stage, treatment; oral contraceptive use; education; history of abortion; and presence of comorbid disease. The estimated values, standard errors, and p values for each variable are given (Supporting Information: Appendix  C.1 ). By the purposeful variable selection method, first testing the significance of each variable at a 25% level of significance, then by only the variables significant at this level could fit the multivariable Cox PH model.

In Table  3 , the Schoenfeld residuals and survival time do not have a statistically significant correlation. This suggests that the 0.05 threshold of significance for the GLOBAL test's “ p  < 0.86” is not significant and that all the factors satisfy the proportionality assumption. Therefore, the Cox model's PH assumption is not broken, according to this. The proportionality presumption is valid because it is presumed that the hazard ratios will stay unchanged throughout time. Therefore, for the survival part of this study, the Cox PH model was used.

The graphical inspection in Figure  2  shows that there is no pattern with respect to time. The PH assumption appears to be supported by covariates such as weight, comorbidity, smoking, history of abortion, and oral contraceptive use. Since the PH assumption had not been violated, the Cox PH model was employed to assess the time‐to‐event data.

Scaled Schoenfeld residual plot for some selected predictor variables, University of Gondar Referral Hospital, 2018–2022.

In Table  4 , in the Cox regression model analysis, factors that had a statistically significantly positive association with time to death were oral contraceptive use, HIV, late‐stage, surgery, squamous cell carcinoma, comorbid disease, and a history of abortion.

Cox PH model estimates of outpatients with cervical cancer.

Abbreviations: CI, confidence interval; HIV, human immunodeficiency virus; HR, hazard ratio; PH, proportional hazard; ref., reference category.

In Table  5 , the finding demonstrates that the change in tumor size was statistically significant correlated with the predictors of visit time, treatment, weight, cancer stage, HIV, oral contraceptives, history of abortion, and smoking status. Additionally, the results show that the predictors of surgery, oral contraceptives, cancer stage, HIV, weight, history of abortion, and comorbid diseases had a highly statistically significant relationship between the risk of death of outpatients with cervical cancer and the survival process. Tumor size and risk of death of outpatients with cervical cancer were simultaneously influenced by HIV, cancer stage, treatment, weight, history of abortion and oral contraceptive use. In the survival sub‐model under joint analysis, the estimate of the association parameter (α) was statistically significantly different from zero, which, in line with our findings, gives strong support for a relationship between the two outcomes. The estimation of the association parameter results indicates that tumor size has a statistically significant positive relationship with the risk of death in outpatients with cervical cancer.

Joint model estimates of outpatients with cervical cancer

Note : Bold values indicate that the p ‐values are significant.

Abbreviations: CI, confidence interval; HIV, human immunodeficiency virus; ref., reference category.

A unit centimeter square rise in tumor size, corresponding to an exp(0.8502) = 2.34 times, significantly raised the mortality risk. The joint model's results in Table  5 show that there is a statistically significant relationship between the change in tumor size and mortality risk due to cervical cancer.

The parameter estimates for the individual and joint models are roughly similar but not identical; therefore, we must compare the standard errors of the two models separately and together for relevant predictors. Table  5 demonstrates that the joint model has lower standard errors for all significant predictors when compared to the separate models. The significant predictors in the joint model's survival submodel were statistically significant relationships with the risk of death, just like they were in the separate survival model in Table  5 , but the joint model's standard error was much lower. The significant variables in the longitudinal submodel model with a joint model have a smaller standard error than the significant factors in the separate longitudinal model. In terms of low standard errors, the joint model fared generally better for this investigation than a separate model. As shown in Table  5 , the estimation of the association coefficient in the survival sub‐analysis of the joint model was not equal to 0. This suggests that two outcome variables are correlated and this helps us to make valid inferences and conclusions; the joint model was better to fit the data, and there is a statistically significant and nonignorable difference due to the measurement error of tumor size.

In Table  5 , both joint models and separate analyses use a random effect. This demonstrates that the variation of random intercepts was greater than the variance of random slopes, pointing to a more significant baseline difference. The correlation coefficient between the random intercept and the random slope is also shown in the two model results. This demonstrates that this shows that slopes and random intercepts are correlated, demonstrating that each individual's slope and intercept are correlated with one another. As a result, the correlation between slopes and intercepts was 0.4250, indicating a positive correlation between intercept and slope of linear time, and the variability within patients was 0.2825 in the joint model. The variability between patients in intercept was therefore 0.5034, and the variability between patients in slope was 0.0116. About 76% of the variation in tumor size that is not explained by predictor variable is attributable to subjects.

The estimated coefficient value of the fixed effect intercept, which can be calculated by removing all covariates from the model, was calculated as 4.5716, meaning that the anticipated change in tumor size for the outpatient with cervical cancer was 4.5716 cm 2 .

The estimated tumor size change of cervical cancer patients was statistically significant decrement by 0.0098 cm 2 for a 1 kg rise in weight, all other factors remaining constant.

Keeping all other factors constant, the estimated tumor size changes in HIV‐positive cervical cancer patient by 0.4360 cm 2 higher than HIV‐negative outpatients with cervical cancer. While controlling for all other factors, the estimated tumor size change of outpatients with cervical cancer in the late stage was substantially higher by 0.2226 cm 2 than that of early stage outpatients with cervical cancer at an early stage.

The predicted tumor size change in outpatients with cervical who received chemotherapy treatment was substantially greater by 0.1624 cm 2 compared to outpatients with cervical cancer who received radiotherapy treatment, with all other factors being constant. The expected tumor size change in outpatients with cervical who had surgery treatment was significantly higher by 0.1841 cm 2 compared to the outpatients with cervical cancer who had radiotherapy treatment alone, all other factors being constant.

When all other factors were held constant, the estimated tumor size change of outpatients with cervical who used an oral contraceptive was considerably greater by 0.2920 cm 2 than it was for outpatients with cervical who did not use an oral contraceptive. When all other factors were held constant, outpatients with cervical cancer who had a history of abortion had an estimated tumor size change that was considerably greater by 0.2376 cm 2  than those with no such history.

When all other factors were held constant, the estimated tumor size change of outpatients with cervical with smokers was 0.3003 cm 2 , which was significantly larger than it was for outpatients with nonsmokers. The average progression of tumor size from a longitudinal process was significantly negatively affected by visit time in this investigation. The average tumor size of outpatients with cervical would decrease by 0.0084 if the follow‐up period was extended by one unit. This suggests that the individuals who received longer follow‐ups experienced a specific decrease in tumor size. The severity of the condition rises as the number of monthly follow‐up visits decreases.

The estimated hazard ratio of weight for cervical cancer patients exp(−0.2072) = 0.8, which indicates that the risk of death for a 1 kg increase in weight was decreased by 20% than the risk of death for a 1 kg decrease in weight, all other factors remaining constant.

The estimated hazard ratio of death for cervical cancer patients who had surgery treatment relative to cervical cancer patients who had radiotherapy treatment was exp(0.2343) = 1.264. The risk of death of outpatients with cervical cancer who had surgery treatment was increased by 26.4% compared to the risk of death for cervical cancer patients who had radiotherapy treatment, keeping all other factors constant.

The estimated hazard ratio of death of outpatients with cervical cancer who had a late stage relative to cervical cancer patients who had early stage was exp(0.1721) = 1.188. The risk of death of outpatients with cervical cancer who had a late stage was increased by 18.8% compared to the risk of death of outpatients with cervical cancer who had an early stage, keeping all other factors constant.

The estimated hazard ratio of death of outpatients with cervical cancer who had HIV positive relative to outpatients with cervical cancer who had HIV negative was exp(0.4636) = 1.59. The risk of death of outpatients with cervical cancer who had HIV positive was increased by 59% compared to the risk of death of outpatients with cervical cancer who had HIV negative, keeping all other factors constant.

The estimated hazard ratio of death of outpatients with cervical cancer who used an oral contraceptive compared to outpatients with cervical cancer who did not use an oral contraceptive was exp(0.6094) = 1.84. The risk of death of outpatients with cervical cancer who used an oral contraceptive was increased by 84% compared to the risk of death of outpatients with cervical cancer who did not use an oral contraceptive.

The estimated hazard ratio of death of outpatients with cervical cancer with a comorbid disease compared to outpatients with cervical cancer without comorbid disease was exp(0.70) = 2.01, meaning that the risk of death of outpatients with cervical cancer with a comorbid disease was 2.01 times higher than the risk of outpatients with cervical cancer with no comorbid disease, all other factors being constant.

The estimated hazard ratio of death for cervical cancer patients with an abortion history compared to outpatients with cervical cancer without an abortion history was exp(0.512) = 1.67, which means that, when all other factors were held constant, the risk of death was increased by 67% of outpatients with cervical cancer with an abortion history.

To validate the assumptions behind the longitudinal submodel and the survival submodel, we usually use common types of residual plots. The fitted joint model's default diagnostic plots for cervical cancer patients undergoing follow‐up from 2018 to 2022 are displayed in Figure  3 . In the top left panel, the longitudinal submodel's subject‐specific residuals and their associated fitted values are displayed. There is little doubt that the residuals closely resemble the fitted line. The constant variance assumption is supported by the plot's lack of any identifiable systematic structure. In the upper right panel, a typical Q–Q plot shows the standardized residuals of the longitudinal process. The points either fall far from the straight line or are dispersed. As a result, we can say that the longitudinal submodel's assumption of the error term's normality was met.

Diagnostics plot for fitted Joint model of outpatients with cervical cancer, University of Gondar Referral Hospital, 2018–2022.

The bottom left plot of the marginal survival versus time indicates that the survival probability is decreasing as time increases. According to the bottom right plot of the marginal cumulative hazard plot, the cumulative hazard is increasing as the time increases.

To assess the overall goodness‐of‐fit test of the longitudinal submodel of the joint model, a scatter plot of the two types of residual conditional (subject‐specific) and average population (marginal) versus the corresponding fitted values can be employed. Figure  4 below compares the marginal residuals and subject‐specific to the fitted value of the longitudinal submodel model. Homoscedasticity and normality assumptions can be verified using these residuals, which also predict conditional errors. Because subject‐specific residuals were clustered around zero and there is no consistent trend in subject‐specific residuals versus fitted, the model assumptions provide a good fit for the data. The marginal residual versus fitted values graphics are concentrated with 0. It shows that the longitudinal submodel in the joint model assumptions was satisfied and successfully fitted. Using Q–Q and histograms, the longitudinal model's initial assumptions about the longitudinal outcome's normality were evaluated. Based on the above‐mentioned mentioned graph, it can be shown that the real tumor size satisfies the assumption of normality without transformation. As a result, we used the original actual data.

Diagnostics plot for longitudinal submodel from the joint model, University of Gondar Referral Hospital, 2018–2022.

To check the PH assumption of the Cox PH model of the survival submodel, the Schoenfeld residuals and the formal statistical test were displayed. The Cox PH assumption for the survival submodel of the time to death among outpatients with cervical cancer was checked graphically by Schoenfeld residuals. Systematic departures from the horizontal line indicate Cox PH model was not appropriate, since it assumes that the estimates of the predictors do not vary much over time. In the plots of Schoenfeld residuals against time, all the significant covariates on the time to death of outpatients with cervical cancer showed randomness and the smooth curve was approximately horizontal straight line, this result was an implication of zero slope. So, all significant predictors included in the survival submodel had zero slopes (the curve exhibits no departures from the origin). Further from graphical tests, the global test was conducted using the covariates in the model. Since the global test was statistically insignificant at the 5% level of significance, the proportionality assumption of the Cox PH model was satisfied. Figure  5 demonstrated model diagnosis based on Cox–Snell residuals with 95% CI for the KM estimate of the Cox–Snell residuals along the red line. This result indicated that the survival process model fitted the data well.

Diagnostics plot for survival submodel from q joint model, University of Gondar Referral Hospital, 2018–2022.

4. DISCUSSION

The objective of this investigation was a joint model of longitudinal tumor size change and time to event (death) of outpatients with cervical cancer at the UGRH, Gondar, Ethiopia.

In our results, the variable weight, stage, contraceptive use, comorbid disease, HIV, treatment, and history of abortion had a significant effect on tumor size and time to event (death) of outpatients with cervical cancer at the UGRH jointly.

For this study, based on the data obtained from the UGRH, 118 (36.6%) patients died. This is lower compared to a research article conducted in Ethiopia; among 346 patients, 223 (64.4%) of them died. 40

Accordingly, the stage of the disease also had a significant association with both risk of mortality and tumor size of outpatients. The risk of mortality of outpatients with cervical cancer who had a late stage was increased by 18.8% compared to the risk of mortality of outpatients with cervical cancer who had an early stage. This outcome is consistent with research done in Ethiopia. 41

According to the findings of the study, oral contraceptive use was a highly significant predictor of tumor size and time to event (death) of outpatients with cervical cancer in the UGRH. Outpatients with cervical cancer who used oral contraceptives had an increase of 84% compared to the mortality risk of those who did not use oral contraceptives. This outcome coincides with the result of Smith et al. 42

According to the findings of the study, the presence of HIV was a strong predictor of both the tumor size and the risk of death of outpatients with cervical cancer at the UGRH. The risk of mortality of outpatients with cervical cancer with HIV was increased by 30% compared to the risk of mortality for outpatients with cervical cancer without HIV. This happens because cervical cancer makes viral load counts higher and they are more likely to die. This result coincides with Gurmu 43 and Seifu et al. 40

The results of this study indicated that the history of abortion was a significant predictive factor for both tumor size progression and time to event (death) of outpatients with cervical cancer at the UGRH. The risk of death of outpatients with cervical cancer who had a history of abortion was increased by 67% compared to the risk of death of outpatients with cervical cancer who had no history of abortion. This result coincided with Gurmu. 43

The results of this study suggested that comorbid disease was a significant predictive factor for the survival time of the patients. Outpatients with cervical cancer without comorbid diseases had a longer survival time than those with comorbid diseases. The risk of death for cervical cancer patients who had a comorbid disease was 2.01 times higher than the risk of death for cervical cancer patients who did not have a comorbid disease. This result coincided with that of Mebratie et al. 44

In our result, education and histology type have an insignificant effect on both tumor size and time to death. This is in contradiction with Mebratie et al. 44 and Getahun et al., 45 respectively.

5. CONCLUSION

In this research, we verified a longitudinal model for tumor size of outpatients with cervical cancer, a Cox PH model for time to event (death), and a joint model for the two outcomes variables together were used.

There is no discernible difference in the time to event (death) between the groups of residency and education, according to the results of the KM curve and log‐rank test. The KM curve showed that nonsmokers had a higher likelihood of surviving than smokers. Similar to this, the KM curve plot for contraceptive use demonstrates that outpatients who do not use oral contraceptives have a higher chance of living than those who do. The joint model performs better at pinpointing the variables associated with the concurrent measurements of tumor size and time to event (death) based on the standard error, CI, and association value.

Based on the results, the variables HIV, oral contraceptive use, stage of cancer, weight, history of abortion, and treatment were statistically significant factors of tumor size and time to death of outpatients with cervical cancer.

The variable longitudinal measure of tumor size has an association with time to death; hence, the joint model is the recommended one for such kinds of correlated data.

Based on the findings, we suggest some recommendations to the concerned body: to address the problems, especially vulnerable outpatients with cervical cancer who used oral contraception, who were HIV positive, and who have a comorbid disease, the health professionals should have continuous health checkups and timely medical care so as to minimize the risk of deaths. Both governmental and nongovernmental organizations should allocate adequate funding for cervical cancer treatments to promote women to get access to CCS, detection, and also full medication purposes to reduce the risk factor of cervical cancer. Health professionals give attention when a patient's estimated tumor size is increased through follow‐up, oral contraceptive use, HIV positive, history of abortion, or late stage. Finally, the researcher suggested that this work can be expanded in the future by integrating significant variables that were not examined in this particular study.

6. LIMITATIONS

The main limitation of the study was that some predictors such as the number of sexual partners, age at first sexual intercourse, and others were not available due to the retrospective nature of the data.

AUTHOR CONTRIBUTIONS

Aragaw E. Aguade : Conceptualization; data curation; formal analysis; investigation; methodology; project administration; resources; supervision; visualization; writing—original draft; writing—review and editing. Chalachew Gashu : Conceptualization; data curation; formal analysis; investigation; methodology; project administration; resources; supervision; visualization; writing—original draft; writing—review and editing. Tigist Jegnaw : Conceptualization; data curation; formal analysis; investigation; methodology; supervision; writing—review and editing.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflict of interest.

ETHICS STATEMENT

All methods are performed according to the relevant regulations and guidelines of the journal. The ethical letter was taken from the University of Gondar, College of Natural and Computational Sciences Ethical Committee with reference no. CNCS/10 976/11/05/2022 and the committee approved the study. The University of Gondar Referral Hospital ethical review board waived the intended consent of individual patients on February 3, 2014 because we used secondary data from hospital patients' medical cards (charts).

TRANSPARENCY STATEMENT

The lead author, Aragaw Eshetie Aguade, affirms that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.

Supporting information

Supplementary information.

ACKNOWLEDGMENTS

The authors are thankful to the University of Gondar Referral and Teaching Hospital for providing us with sufficient data for our study.

Aguade AE, Gashu C, Jegnaw T. The trend of change in cervical tumor size and time to death of hospitalized patients in northwestern Ethiopia during 2018–2022: retrospective study design Health Sci Rep . 2023; 6 :e1121. 10.1002/hsr2.1121 [ CrossRef ] [ Google Scholar ]

DATA AVAILABILITY STATEMENT