Skip to main content
Erschienen in: BMC Public Health 1/2021

Open Access 01.12.2021 | Research

Determinants and levels of cervical Cancer screening uptake among women of reproductive age in South Africa: evidence from South Africa Demographic and health survey data, 2016

verfasst von: Monica Ewomazino Akokuwebe, Erhabor Sunday Idemudia, Abiel M. Lekulo, Ogone Warona Motlogeloa

Erschienen in: BMC Public Health | Ausgabe 1/2021

Abstract

Background

Cervical cancer (CC) is the cancer with the most incidents and the leading cause of cancer mortality among women in South Africa. CC screening is one of the most cost-effective control approaches for the disease burden. This study assessed the determinants and individual-level indicators of cervical cancer screening uptake among women of reproductive age in South Africa.

Methods

We analyzed data from the 2016 South Africa Demographic Health Survey. Our analysis focused on 5903 women (15–49 years). We conducted Chi-square test for bivariate analysis, and multivariate binary logistics regression was used to analyze independent association between individual-level factors and women who have had Pap smear testing. Statistical significance was set at p < 0.05.

Results

The mean age at cervical cancer screening uptake among women in South Africa was 40.8 years (SD 18.6, range 15–95 years). A majority of the women (39.3%) were aged 45 years and above and 54.6% of them resides in urban settlements. About 35.4% of women (n = 2098) have had a Pap smear test, with 66.5% of them who had a Pap smear test resides in Western Cape province. The proportion of women who had a Pap smear test was significantly higher among those with higher educational attainment (68.7%, p = 0.000), in the rich wealth index (50.1%, p = 0.000), and those with health insurance cover (60.3%, p = 0.000). Pap smear testing was found to be more prevalent among women aged 45+ years, were in the white population group, had higher education, were divorced, and had health insurance cover. The predominance of Pap smear test was 14% higher among women who are working in the professional/formal sector (AOR; 1.38, 95% CI; 1.14–1.69). The uptake of Pap smear test was also higher among women aged 35–44 years.

Conclusions

The prevalence of cervical cancer uptake is substantially low among women aged 15–24 years in South Africa and shows a degree of between-provinces differences. Therefore, heath educational interventions aimed at increasing the uptake of cervical cancer screening services in South Africa are critically needed.
Hinweise

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Abkürzungen
CC
Cervical cancer
AOR
Adjusted odds ratio
CI
Confidence interval
HPV
Human papilloma virus
ORs
Odds ratio
SADHS
South Africa demographic health survey
Adjusted
A
Unadjusted
U
DNA
Deoxyribonucleic acid
STATA
Statistical analysis software
SSA
Sub-Saharan Africa
RC
Reference Category

Background

Cervical cancer is a serious public health problem and is one of the second leading causes of cancer-related mortality among women worldwide. Its epidemiology and health impacts are not only affecting women, but also their families, communities and social institutions [1]. Although it is also one of the most preventable disease through proper screening, treatment and follow-up, more than half a million women worldwide develop intrusive cervical cancer each year [2]. Middle- and low-income countries bear an unequal share (83%) of the global cervical cancer burden, but only achieve an average successful screening coverage of 19%, compared to 63% in high-income countries [3]. Studies [46] have accounted for over 275,000 female deaths and approximately 529,000 new diagnoses each year; besides, cervical cancer disease burden is more prevalent in older women who are post-childbearing [712]. In the developing countries, lack of resources limits coverage of cervical screening for women [1315], and notably, for those from rural communities compared with urban areas, as the rural population is extensively poor and their access to health services is more difficult [1622]. Overall, developed countries such as the United States of America (USA) and United Kingdom, 40 and 42% of the women diagnosed with cervical cancer respectively, die from it [7, 10, 11, 22, 23], while in Africa and South Asia, the equivalent death rates are nearly twice (78%) as high as the rates experienced in high-income countries [23, 24].
In sub-Saharan Africa, cervical cancer encompasses 20–25% of all cancers among women. The estimate is double that of women globally, as its incidence ranges from 30 to 40 per 100,000 women [24]. In South Africa, cervical cancer is the cancer with the most incidents and the leading cause of cancer mortality among women [25]. Contemporary estimates have shown that every year in South Africa, 5743 women are diagnosed with cervical cancer and 3027 die from the disease. Also, it is the second most frequent cancer among women of reproductive age between 15 and 44 years of age, after breast cancer. Studies [2628] have shown that young women are at higher risk as they tend to be sexually active and have higher numbers of sexual partners. Several studies [8, 26, 27] have reported that young women are poorly informed about cervical cancer with its associated risk factors, and are unclear about the intent of cervical cancer screening, as well as holding on to negative or inaccurate beliefs or attitudes to Pap testing. Furthermore, one of the known main causative agents in cervical cancer is HPV and there are over 200 recognized serotypes of the HPV virus. Existing studies [29, 30] have documented that about 21.0% of women in the general population of South Africa are estimated to harbor cervical HPV infection in South Africa. These reports have shown that 62.8% of invasive cervical cancers among women in South Africa are attributed to HPVs 16 or 18 [29], which fall in the high-risk HPV serotypes classification, and which are responsible for almost 70% of cervical cancer cases.
Other factors for increasing young women’s susceptibility to cervical dysplasia (dysplasia is defined as medically unusual growth or unusual development or growth of a part of the body such as an organ, bone or cell, including the total absence of such a part) include smoking, oral contraceptive use, and vulnerability of the adolescent cervix to sexually transmitted infections [3133]. As a consequence of the sexually transmitted nature of HPV, early exposure to sexual intercourse and multiple sex partners are significant risk factors for cervical cancer [5, 34]. Studies have reported that 80–90% of women will have this sexually transmitted infection at some point in their life, although only 3–4% of them will develop cervical cancer [35, 36]. Earlier studies [29, 37] have indicated that the South African Cancer Association (SACA) report in the year 2006 revealed that the age-standardized incidence rate for cervical cancer was 24.71 per 100,000 population. As a result of SACA reports, the South African Department of Health developed the Cervical Cancer Screening Programme, which allows three Pap smears per lifetime, at 10-year intervals, starting at the age of 30. This screening policy programme was designed for target coverage of at least 70% of women nationally [37].
Even with the implementation of the Cervical Cancer Screening Policy Programme in South Africa, the screening coverage is 20%, nationally low for women over the age of 30 years [38]. A population-based study conducted among rural South African women reported that only 18% of the women had ever had a Pap smear test [39]. Another study conducted among female university students found that 42.9% of the participants had heard of cervical cancer, but only 9.8% of the participants had ever had a Pap smear test [40]. Another study conducted in Vhembe District of South Africa, reported that campaigns and motivational talks on cervical cancer as well as cervical cancer screening services are provided for women in all the clinics in the district [41], yet very few women voluntarily present themselves for cervical cancer screening services.
Moreover, women who utilized the cervical cancer screening services do so because they have been referred by other health facilities, or the women are presenting with symptoms. Factors that are associated with poor uptake of cervical cancer screening services are pain, stigmatization, and fear of embarrassment [4244], time constraint [25, 45], the related costs [25, 42, 45], insolence of health workers [46], lack of awareness about where to get screening [25, 47] and delays in hospital cancer screening [25]. Therefore, cervical cancer becomes a public health burden in countries where there are no cervical cancer screening services, or poor utilization of screening services. Cervical cancer screening services could be utilized better if awareness campaigns are sustained and the services are accessible, affordable and available [48]. Early screening is proven to be cost-effective and a form of control strategy of the disease burden [6, 33]. Thus, early screening of cervical cancer is an important preventative strategy for the disease burden. Improving screening services will not be sufficient to result in increased screening uptake among women, unless we understand and address the multidimensional causes that are likely to impel women’s disposition towards cervical cancer screening. Very little is known about determinants and levels of cervical cancer uptake among women of reproductive age in South Africa. No previous study conducted in South Africa has investigated the determinants and levels of cervical cancer uptake among women of reproductive age (15–49 years) in South Africa. The objectives of this study were to examine the association between determinants and cervical cancer uptake at the individual- and community-factor levels using a logistic statistical model, and to assess the extent of the variation in the uptake levels of cervical cancer screening services in South Africa. The findings of this study will provide insight into the provision of appropriate educational interventions for disease risk reduction and effective cervical cancer screening uptake among women of reproductive age in South Africa.

Methods

Study setting

South Africa, officially the Republic of South Africa (RSA), covering 471,445 km2, has a population of approximately 59.62 million people, comprising diverse cultures, religions, origins and languages [49]. South African culture is not homogeneous but rather a collection of cultures, with different cultures being predominant in different regions. The country has an upper middle-income economy identified as newly industrialized country [50]. However, poverty and inequality remain widespread, with about a quarter of the population unemployed and living on less than US$1.25 a day. The country has been identified as a middle power in international affairs, and maintains a significant regional influence [50]. However, wide differences exist in the political and administrative economy of the country, with nine provinces: Western Cape, Eastern Cape, Northern Cape, North West, Free State, KwaZulu-Natal, Gauteng, Limpopo and Mpumalanga [51]. Most provinces, except Limpopo, have high levels of socioeconomic development and tourist attractions in terms of infrastructure, industries and services. Limpopo province is a known typical developing area, with export and import of primary products and manufactured goods and services, as well as a large platinum deposit. Yet it is one of the poorest regions of South Africa, with a big gap between poor and rich residents, especially in rural areas [51].
The country operates a three-tier system of government (Legislative, Executive and Judicial) with an independent judiciary operating in a parliamentary system. The provincial governments of the nine provinces of South Africa have their own executive and legislative branches, but not separate judicial systems [49], while the local government consists of municipalities of various types. The largest metropolitan areas are governed by metropolitan municipalities, while the rest of the country is divided into district municipalities, each of which consists of several local municipalities [49]. This synopsis of political economy underlines vital aspects of culture and contextual influences on people’s lifestyles and behaviours.

Data and sample

This study used data from the most recent 2016 South African Demographic and Health Survey (SADHS) [51], conducted in South Africa, which is the third DHS, and follows the surveys carried out in 1998 and 2003. The SADHS is a nationally representative survey dataset conducted and collected as a collaboration between Statistics South Africa (Stats SA), the South African Medical Research Council (SAMRC) and the National Department of Health (NDoH), with technical support from ICF through the DHS Program of the United States Agency for International Development (USAID). The survey was designed to provide representative estimates for main demographic and health indicators for the country as a whole, for urban and non-urban areas separately, and for each of the nine provinces in South Africa.
A two-stage stratified sampling design was applied that involved randomly selecting the sampling clusters that were created in the first stage, followed by randomly selecting households in the second stage. Implicit stratification and proportional allocation were achieved at each of the lower administrative levels within a given sampling stratum by sorting the sampling frame according to administrative units at different levels in each stratum and using probability proportional to size selection at the first stage of sampling. Questionnaires were pre-tested to ensure that the questions were clear and could be understood by respondents. Our analysis focused on women of reproductive age (15–49 years) in 5903 clusters who were interviewed face-to-face about cervical cancer.

Measures

Outcome variables

The outcome variable for this study is a Pap smear (Pap smear test is one of the types of test used in cervical cancer screening that is carried out on a sample of cells from the cervix to check for abnormalities that may be indicative of cervical cancer) uptake, which is a binary variable whereby the respondents were asked if they have had a Pap smear test. Specifically, respondents were asked “Have you ever been tested or examined for cervical cancer?” (No/Yes). Respondents who answered “Yes” were then asked “Whether they ever had a Pap smear?”

Individual-level variables

Individual-level variables at the micro level included were twenty: women’s age (15–24, 25–34, 34–44 and 45+ years), population group (Black African, White, Coloured, and Indian/Asian), province (Western Cape, Eastern Cape, Northern Cape, Free State, KwaZulu-Natal, North West, Gauteng, Mpumalanga, and Limpopo), place of residence (urban and rural), educational level (no education, primary, secondary, and higher), occupation (not working, professional/formal, and non-professional/informal), marital status (never married, married, divorced, and widowed), health insurance cover (yes, and no) and own health perception (poor, average, good, and excellent). The household wealth index was a composite score measured by ownership of household items and facilities based on a DHS-generated quintile index and was categorized as poorest, poorer, middle, richer and richest. The quintile index for poorest and poorer was merged as poor wealth index; and richest and richer was also merged as rich wealth index. In this study, the principal investigators re-categorized the merged DHS-generated quintile index as poor, middle and rich wealth index.

Community-level variables

Geographical type and provinces were non-aggregate community-level variables. Geographical type was recorded as urban and rural. Provinces were defined as the region where a woman comes from. Basically, South Africa is demarcated into nine provinces: Western Cape, Eastern Cape, Northern Cape, Free State, KwaZulu-Natal, North West, Gauteng, Mpumalanga, and Limpopo, and the living status of their population, and settings may have a relationship with cervical cancer screening uptake. Another group of community-level variables were constructed through an aggregation from individual-level using an average approaches to conceptualize the neighborhood effect on cervical cancer screening uptake by women of reproductive age. The other group of community-level variables were: women’s age, population group, province, place of residence (urban and rural), educational level, occupation, marital status, health insurance cover, own health perception, and wealth index.

Statistical analyses

Data were weighted to give an explanation for multistage sample design, and analysed using Stata 14 (StataCorp, 2017). Univariate analysis illustrated frequencies and percentages for socio-demographic variables. Cross-tabulations of each independent variable and ever had a Pap smear were applied for inferential analysis. A chi-squared test ascertained whether there was any association between population characteristics and ever had a Pap smear. Multivariate binary logistics regression using variables whose univariate analysis was significant was used to estimate the independent association between respondents who have had Pap smear testing and population characteristics. Unadjusted and adjusted models were constructed in the logistics binary regression, and only individual variables were included to bring out interested findings for this study. Hence, the odds ratios (ORs) for the binary logistic regression with 95% confidence intervals (95% CIs) were reported.

Ethical considerations

All data were obtained from the 2016 SADHS. Informed consent was obtained from each respondent before the interviews (2016 SADHS). We obtained approval to use the data from the DHS repository (http://​dhsprogram.​com/​data/​available-datasets.​cfm).

Results

Table 1 shows the socio-demographic characteristics of women of reproductive age with a total of 5903 who participated in the study. From the table below, 35.5% of women indicated that they have had a Pap smear test, and 64.5% of them reported that they have not had a Pap smear test. The mean age at cervical cancer screening among women in South Africa was 40.8 years (SD 18.6, range 15–95 years). Most women were 45+ years (39.0%) followed by 15–24 years (23.6%) who participated in the survey. A majority of the women were from the African/Black population group (84.9%), with the Indian/Asian population group having the least (1.3%). Out of all the women interviewed, 15.9% of the respondents were from KwaZulu-Natal province, followed by 14.1% from Limpopo province. More women were from the urban areas (54.6%) than rural areas (45.5%) (Table 1).
Table 1
Distribution of Population by Socio-Demographic Characteristics, South Africa
Socio Demographic Characteristics
Frequency
Percentage
N = 5903
100
Ever had Pap Smear
Yes
3805
35.5
No
2098
64.4
Age Group
15–24
1394
23.6
25–34
1268
21.5
35–44
937
15.9
45+
2304
39.0
Population Group
African/Black
5010
84.9
White
251
4.3
Coloured
566
9.6
Indian/Asian
76
1.3
Province
Western Cape
445
7.5
Eastern Cape
779
13.2
Northern Cape
495
8.4
Free State
637
10.8
KwaZulu-Natal
941
15.9
North West
561
9.5
Gauteng
547
9.3
Mpumalanga
666
11.3
Limpopo
832
14.1
Geographical Type
Rural
2683
45.5
Urban
3220
54.6
Educational Attainment
No education
569
9.6
Primary
1018
17.3
Secondary
3776
64.0
Higher
540
9.2
Occupation
Not working
4127
69.9
Professional/Formal
1020
17.3
Non-professional/Informal
756
12.8
Marital Status
Never Married
3667
62.1
Married
1461
24.8
Divorced
113
1.9
Widowed
662
11.2
Wealth Index
Poor
2430
41.2
Middle
1317
22.3
Rich
2156
36.5
Health Insurance Cover
Yes
796
13.5
No
5107
86.5
Perceived Health Status
Poor
766
13.0
Average
1980
33.5
Good
2384
40.4
Excellent
773
13.1
Source: SADHS, 2016
The majority of the respondents had secondary education (64.0%) and 17.3% of them have primary education. Among the women interviewed, 69.9% of the women are not working while 17.3% work in the professional/formal sector and 12.8% work in the non-professional/informal sector. Three thousand six hundred and sixty-seven (62.1%) of them have never been married; most (41.2 and 36.5%) were in the poor and rich wealth index categories respectively (Table 1). The majority (86.5%) of the women do not have health insurance cover and 40.4% perceived themselves to have good health status.
Table 2 presents the results of the bivariate analysis of the individual-level characteristics and Pap smear testing. In the bivariate analysis, all individual-level variables (age group, population group, province, geographical type, educational attainment, occupation, marital status, wealth index, health insurance cover and perceived health status) were significantly associated with women’s responses to cervical cancer screening (Pap smear test). Regarding the age group showing the most significant association with Pap smear testing (χ2 = 724.93, p = 0.000), a majority of women (52.5%) in age cohorts of 35–44 years have undertaken a Pap smear test compared to those in other age groups.
Table 2
Population Characteristics by Pap Smear Testing among Females Aged 15–49 Years in South Africa
Ever had a Pap Smear
Population Characteristics
No
Yes
Total
5903
N
%
N
%
Women’s age group
χ2 = 724.9315; p = 0.000
 15–24
1291
92.6
103
7.4
1394
 25–34
839
66.2
429
33.8
1268
 35–44
445
47.5
492
52.5
937
 45+
1230
53.4
1074
46.6
2304
Population Group
χ2 = 306.7635; p = 0.000
 African/Black
3442
68.7
1568
31.3
5010
 White
59
23.5
192
76.5
251
 Coloured
273
48.2
293
51.8
566
 Indian/Asian
31
40.8
45
59.2
76
Geographical Type
χ2 = 183.8032; p = 0.000
 Urban
1828
56.7
1392
43.2
3220
 Rural
1977
73.7
706
26.3
2683
Educational Attainment
χ2 = 164.2445; p = 0.000
 No education
434
76.3
135
23.7
569
 Primary
665
65.3
353
34.7
1018
 Secondary
2483
65.8
1293
34.2
3776
 Higher
223
42.3
317
68.7
540
Occupation
χ2 = 238.79335; p = 0.000
 Not working
2903
70.3
1224
29.7
4127
 Professional/Formal
462
45.3
558
54.7
1020
 Non-professional/Informal
440
58.2
316
41.8
756
Marital Status
χ2 = 327.8518; p = 0.000
 Never Married
2649
72.2
1018
27.8
3667
 Married
706
48.3
755
51.7
1461
 Divorced
32
28.3
81
71.7
113
 Widowed
418
63.1
244
36.9
662
Wealth Index
χ2 = 339.9505; p = 0.000
 Poor
1829
75.7
591
24.3
2430
 Middle
891
67.7
426
32.4
1317
 Rich
1075
49.9
1081
50.1
2156
Health Insurance Cover
χ2 = 246.2157; p = 0.000
 No
3489
68.3
1618
31.7
5107
 Yes
316
39.7
480
60.3
796
Source: SADHS, 2016
A large proportion of white women (76.5%) have undertaken a Pap smear test compared to women in the other population groups, and this shows a significant association between population group and Pap smear uptake (χ2 = 306.76, p = 0.000), while educational attainment was found to be significantly associated with Pap smear testing (χ2 = 306.7635; p = 0.000), and 43.2% of urban women have had a Pap smear test compared to their rural counterparts, at only 26.31%.
It can be deduced from the findings that urban women have higher chances of undertaking Pap smear testing, as geographical type was significantly associated with Pap smear testing (χ2 = 183.80; p = 0.000) (Table 2). Figure 1 depicts the proportion of women of reproductive age who have had Pap smear by province. Western Cape Province had the highest proportion (66.52%) of women who have had a Pap smear, while Limpopo province had the lowest proportion of women who have had a Pap smear (Fig. 1).
However, a majority of women (39.95%) who perceived their health status to be poor had taken a Pap smear test compared to those with perceived excellent health status (27.94%) (Fig. 2).
Table 3 presented the multivariate analysis illustrating both the unadjusted (U) and adjusted (A) Odds Ratios (OR) of population characteristics which were found to be significant predictors of Pap smear uptake among women of reproductive age. Women aged 35–44 years were found to have 14 and 12% (UOR: 12.14: 95% CI = 9.36–15.72; AOR = 13.62: 95% CI = 10.56–17.55) higher odds of having a Pap smear compared to those aged 15–24 years, and this was found to be statistically significant. Population group has a significant association with Pap smear uptake as the odds of having a Pap smear among white respondents were 2.2 and 2.5 times (UOR; 2.21, 95% CI; 1.54–3.15; AOR; 2.47, 95% CI; 1.75–3.50) higher as compared to African/Black women. Province was significantly associated with lesser odds of having Pap smear uptake: Gauteng (UOR: 0.24, 95% CI: 0.17–0.34; AOR: 0.24, 95% CI = 0.17–0.33); Limpopo (UOR; 0.30, 95% CI; 0.21–0.43; AOR; 0.30, 95% CI; 0.21–0.42); KwaZulu-Natal (UOR; 0.30, 95% CI; 0.22–0.42; AOR; 0.30, 95% CI; 0.21–0.41).
Table 3
Logistic Regression Showing Odds Estimates of Pap Smear Testing amongst Women aged 15–49 years by Population Characteristics in South Africa
Population Characteristic
Ever had Pap Smear, N = 2098
Model I: Unadjusted AOR
Model II: Adjusted AOR
OR
p > Z
[95% Conf. Interval]
OR
p > Z
[95% Conf. Interval]
Age group
15–24
RC
   
RC
   
25–34
5.61
0.000
4.3862
7.17
6.09
0.000
4.78
7.76
35–44
12.14
0.000
9.3698
15.73
13.62
0.000
10.57
17.55
45+
11.95
0.000
9.2343
15.47
13.06
0.000
10.12
16.85
Population Group
 African/Black
RC
   
RC
   
 White
2.21
0.000
1.54
3.16
2.48
0.000
1.75
3.51
 Coloured
1.05
0.697
0.81
1.37
1.07
0.697
0.82
1.39
 Indian/Asian
1.56
0.107
0.91
2.68
1.63
0.107
0.95
2.80
Province
 Western Cape
RC
   
RC
   
 Eastern Cape
0.40
0.000
0.29
0.55
0.40
0.000
0.29
0.55
 Northern Cape
0.38
0.000
0.28
0.52
0.37
0.000
0.27
0.50
  Free State
0.33
0.000
0.24
0.47
0.33
0.000
0.23
0.45
 KwaZulu-Natal
0.31
0.000
0.22
0.43
0.30
0.000
0.22
0.42
 North West
0.46
0.000
0.33
0.64
0.46
0.000
0.33
0.64
 Gauteng
0.24
0.000
0.17
0.34
0.24
0.000
0.17
0.34
 Mpumalanga
0.41
0.000
0.29
0.57
0.41
0.000
0.29
0.57
 Limpopo
0.31
0.000
0.22
0.43
0.31
0.000
0.22
0.43
Geographical Type
 Urban
RC
   
RC
   
 Rural
0.73
0.000
0.62
0.86
0.72
0.000
0.61
0.86
Educational Attainment
 No education
RC
   
RC
   
 Primary
1.86
0.000
1.46
2.38
1.88
0.000
1.47
2.40
 Secondary
2.72
0.000
2.14
3.47
2.92
0.000
2.30
3.71
 Higher
4.45
0.000
3.20
6.19
5.61
0.000
4.09
7.70
Marital Status
 Never Married
RC
   
RC
   
 Married
1.31
0.000
1.13
1.53
1.33
0.000
1.14
1.54
 Divorced
2.53
0.000
1.60
4.02
2.58
0.000
1.63
4.09
 Widowed
0.90
0.342
0.73
1.12
0.89
0.342
0.72
1.09
Health insurance Cover
 No
RC
       
 Yes
1.37
0.003
1.11
1.69
    
Wealth Index
 Poor
RC
   
RC
   
 Middle
1.12
0.192
0.94
1.33
1.14
0.192
0.96
1.35
 Rich
1.38
0.001
1.14
1.67
1.47
0.001
1.22
1.77
Occupation
 Not working
RC
       
 Professional/Formal
1.38
0.000
1.16
1.65
    
 Non-professional/Informal
1.24
0.016
1.04
1.48
    
Perceived health status
 Poor
RC
       
 Average
0.80
0.025
0.66
0.97
0.82
0.025
0.68
0.99
 Good
0.81
0.040
0.67
0.99
0.84
0.040
0.69
1.03
 Excellent
0.67
0.003
0.51
0.88
0.71
0.003
0.55
0.92
Source: SADHS, 2016; RC – Reference category
Also, educational attainment has a significant association with Pap smear uptake, as the odds of being screened for cervical cancer among women having secondary and higher education were 2.7 and 4.4 times higher as compared to women who have no education (Table 3). Women who had health insurance cover had 13% higher odds of having Pap smear uptake compared to those who had no health insurance cover, and this was found to be statistically significant (UOR; 1.36, 95% CI; 1.11–1.68). For occupational status, women who are in the professional/formal sector had 14% higher odds of taking Pap smear test compared to those who are not working (AOR; 1.38, 95% CI; 1.14–1.69).

Discussion

This study examined in an all-inclusive manner the background determinants of the use of cervical cancer screening among women of reproductive age in South Africa, with particular emphasis on individual proportion of geographical type demerit (urban and rural), occupation disadvantage (not working, professional and non-professional), wealth index drawback (poor, middle and rich), health insurance cover (yes and no), and educational attainment disadvantage (no education, secondary and higher). The study found that unmeasured irregularity in cervical cancer screening routine across age and population groups was significant through peripheral factors, as population characteristics are explained by significant differences. Such significant differences have been observed in several studies, where population characteristics have accounted for specific background unpredictability factors that determine cervical cancer screening utilization among women of reproductive age [6, 52, 53].
Generally, all the background factors for the study were found to be significantly associated with cervical cancer screening uptake at the individual level, a lattice of other factors (Model II). This observation is not unusual when all individual-level variables are considered simultaneously [8, 54, 55]. This is a key finding showing the significance of the multilevel models in examining classified structured datasets of the 2016 SADHS. Further, access to health facilities have been established to be an important determinant of cervical cancer screening among women [28, 32, 56], as population characteristics seem to be more significant in health matters. The identified significant individual-level factors were age group, population group, province, geographical type, educational attainment, marital status, health insurance, wealth index, occupation, and perceived health status. The consequences of these factors in cervical cancer screening uptake are well established in studies conducted in African countries [5, 57].
Our study contributes to the understanding of determinants and levels associated with cervical cancer screening uptake in South Africa, where the cervical cancer screening prevalence remains low [58, 59]. To the best of the authors’ knowledge, this is the first study that assesses population factors associated with cervical cancer screening uptake in South Africa using the 2016 SADHS. Our findings reveal that a significant number of women (64.46%) did not have an uptake of cancer screening; while the small fraction of the female population who had had a Pap smear were majorly found in Limpopo (25.96%) and KwaZulu-Natal (28.27%) provinces. Thus, lack of knowledge, younger age, lack of income, apprehension of Pap smear testing, and poor accessibility of health facilities’ screening services were significantly associated with low cervical cancer screening outcomes [4, 33, 60]. Consequently, in most industrialized countries, cervical cancer screening programmes have shifted from clinician-sampling to self-sampling for HPV testing, which has been proven to be equally accurate in combination with a follow-up Pap smear test. This implies that various health stakeholders can incorporate self-sampling HPV DNA testing into cervical cancer screening health educational programmes, especially at grassroots’ levels. Present studies have recommended self-sampling HPV DNA testing to be feasible, and may significantly improve cervical cancer screening uptake in South Africa [6163].
Our study revealed that the prevalence of women who had Pap smear testing was higher among women with poor perceived health status, and also among those residing in Western Cape and North West provinces, respectively. A possible explanation for the provincial variation observed is that the urban settlements characteristically have higher socioeconomic status, less cultural conservatism, and easier access to health care services [6466]. Corroborating the results of similar studies, our results demonstrate that women’s occupation and wealth index were positively associated with cervical cancer screening [5, 31, 57]. The lower outcome of cervical cancer screening among women of reproductive age may indicate a financial burden, which is a barrier to accessing cervical cancer screening services. Women with higher occupational status were more likely to undergo screening because these groups of women are most likely to own health insurance cover [1, 67]. Our study determined that individual-level factors such as women’s wealth index had a positive influence on cervical cancer screening behaviour and attitude, indicating that gender disparity, as assessed through wealth index, can affect screening services uptake.
Studies have indicated that women do not accumulate properties converted as wealth as much as men, resulting in a gender wealth gap [68, 69], as women are often perceived as passive and powerless; in addition, societies have apportioned wealth and assets ownership as mostly in the male domain. Besides, several myths and misinformation related to women that have undergone cervical cancer screening have been accepted generally [34], and consequently have various health implications among such women who will tend towards denial of life-threatening health problems [20, 21]. Empowering women with the right knowledge of the benefits of Pap smear testing is necessary and key to having prior information about health matters, especially with terminal diseases. Women who resided in urban settlements, comprising a higher proportion of women with secondary and higher educational attainment, were more likely to undergo screening. This finding is consistent with the findings of previous studies, suggesting that communities with a high concentration of educated women can increase the utilization of health care facilities, including cervical cancer screening services [70, 71]. Education is frequently associated with increased access to health care services and improved knowledge regarding health matters and behaviours. Increasing the proportion of educated women may facilitate the dissemination of knowledge and awareness to those with lower education, aiding them in accessing health services through informal social networks and contacts within their community space [18, 69].
Supporting our study objectives and previous findings of other studies [33, 59, 72], we found a positive association between the white female population group and cervical cancer screening. The possible explanation for this unexpected result is that the white population group may have higher expectations for health services and accessibility to health facilities. Other structural reasons may be gaining full access to transportation and finance to access cervical cancer screening services, which can influence screening behaviour among the white population group [33, 60]. Urban women were seen to have undertaken more Pap smear testing than rural women, as geographical type was significantly associated with Pap smear testing. It could be inferred that women in urban settlements may have access to sensitization programmes on Pap smear testing, health facilities and health insurance cover. Women in Western Cape Province were found to have undergone more Pap smear tests than women from Limpopo province. The outlying areas in South Africa play a role in sensitization of women on the benefits of cervical cancer, as these provinces are stratified as urban and rural settlements due to infrastructural facilities put in place in these areas.
Further research should include these potential factors associated with cervical cancer screening in the study design and analysis. As anticipated, health insurance coverage was strongly associated with cervical cancer screening outcomes, as our findings regarding the association between health insurance cover and Pap smear testing are consistent with the outcomes of previous studies [58, 59]. Our study findings prove that the adoption of a universal health insurance scheme ensuring equity in access to health care can largely enhance the possibility of cervical cancer screening use [6]. The cost of a Pap smear test may be a major impediment in cervical cancer screening uptake among women with meagre earnings, as this may further explain the low turn-out for cervical cancer screening among rural women [52, 59]. In a geographical area where poverty is high, alternative health services are given greater priority to out-of-pocket payments than preventive services [53, 59], and consequently, health insurance cover may potentially reduce the financial burden for rural women to have access to preventive health care services, including Pap smear testing.
In line with other studies, this study has shown a positive relationship between perceived health status and uptake of Pap smear testing. Women of reproductive age with consistent upkeep and maintenance may have regular dealings with health facilities and health care workers, including going for a Pap smear test when necessary [1, 59]. Specifically, in constrained settings, interaction with community health personnel after visitation to health facilities may increase women’s exposure to undertake preventive measures and encourage adoption of accurate health information on the benefits of cervical cancer screening [4]. Preceding studies have also validated that having a prescription from a doctor and treatment medic’s prescription and medicament was constantly found to be a strong predictor of adherence to cervical cancer screening [6, 53]. Our study has some prospective limitations. First, the cross-sectional study design restricted our capacity to draw underlying deductions for the relationship of individual-level factors with uptake of a Pap smear test, which require a longitudinal designs, but could not be determined. In addition, due to limited number of variables collected by the 2016 SADHS, we could not examine a full array of factors related to cervical cancer screening, particularly cultural factors including the quality of the health service and other factors related to user-friendliness of cancer screening facilities. The study also suggests the use of ethnographic methods that may unravel community factors that may influence the outcomes of cervical cancer screening.

Conclusion and recommendation

Most women in South Africa demonstrated a low uptake of cervical cancer screening, as utilization of Pap smear testing among women of reproductive age in the study area was 35.5%. Despite that, when compared to previous studies conducted in countries within East Africa (Uganda – 20.6%; Kenya – 12.3%), West Africa (Nigeria – 13.5%; Benin – 0.6%) and Southern Africa (Namibia – 23.6%; Zimbabwe – 17.0%), there is still a high coverage of Pap smear testing among women of reproductive age in South Africa [7377]. As implied in the literature, cervical cancer screening is associated with an increase in demographic factors that will influence the utilization of the services [33, 60]. Although in this study, demographic factors (such as age, educational attainment, health insurance cover, occupation, geographical type, and perceived health status) were significantly associated with utilization of cervical cancer screening services, yet in reality cervical cancer screening uptake is relatively low. Thus, these factors that result in cervical cancer screening services usage vary between individuals and from community to community [8, 54, 55]. The most basic conclusion is that there is a significant variation that exists in the population group and provinces in the use of cervical cancer screening services among women in South Africa.
The selected broad range of individual-level factors was not able to explain contextual variation as there is much more variation in cervical cancer screening among factors related to women’s utilization of cervical cancer screening services. Policies that look at women’s individual characteristics, such as promoting women employment, especially in professional occupations, higher educational level attainment and wealth accumulation, should continue to be implemented in order to increase Pap smear test uptake and achieve the universal health coverage goal. To mitigate those problems, there should be consistent monitoring of the cervical cancer detection and preventive actions among women through sensitization of health education, to modify women’s behaviours and attitude towards adopting cervical cancer screening. Health professionals and community health workers should promote educational and health recreational programmes provided by local councilors for individuals in their respective communities to have a prior knowledge of the dangers of not undergoing Pap smear testing.
Since early case detection through screening is the most cost effective activity for reducing the disease burden, reproductive health workers and policy stakeholders are needed to demonstrate more commitment in creating awareness about cervical cancer. Stakeholders in the Ministry of Health are needed to design and make Pap smear tests free for women through the establishment of more screening centres in different geographical areas of the provinces in South Africa. The existing Pap smear testing programmes mostly provided by non-governmental as well as faith-based organizations, which are majorly located in urban settlements, need to be decentralized and harmonized for greater efficiency in South Africa. Also, there is need to integrate the cervical cancer screening exercise into the mainstream health care services in the medical institutions. Women who are at least 15 years of age, particularly those with a family history of cervical cancer, must be encouraged to opt for cervical cancer screening at every available opportunity. Lastly, there is need to increase the number of medical professionals and community health workers with the requisite skills to conduct cervical cancer screening in South Africa.

Implications for practice and/or policy

Our findings suggest that the implementation of health educational policies promoting cervical cancer screening through awareness and sensitization programmes can enhance the uptake of the testing by women. Thus, employment programmes should be targeted to provide occupation and job opportunities among women, as instituting income-generating programmes may intensify women’s intent in uptake of screening services. In addition, the impact of expanding improved health insurance coverage could be considerable. Health insurance coverage can possibly aid in the reduction of out-of-pocket health expenses for women of reproductive age, and empower them financially to claim and be able to access cervical cancer screening services. Also, health policymakers should address the problem of geographical disparities in the uptake of Pap smear testing; this can be achieved through effective approaches such as building up better cancer screening health facilities and health workers in rural settlements to minimize geographical inequity. Public health programmes must be intensified to target women of childbearing age about the advantages of early detection of cervical cancer and to encourage them to adopt preventive behavioural modifications. Furthermore, to increase the improvement of the overall coverage of Pap smear testing in order to attain optimum safeguarding of themselves against cervical cancer burden, self-testing and collecting samples of human papilloma virus can be a possible proposition for cervical cancer screening in future policy development.

Acknowledgements

We give thanks to the MEASURE DHS for providing us with the population-based dataset through their archives which can be downloaded from http://​dhsprogram.​com/​data/​available-datasets.​cfm. The authors acknowledge Mrs. Helen Thomas for her editing role. The authors also gratefully acknowledge the support of the North-West University Faculty of Humanities, Mafikeng, South Africa.

Declarations

All data were obtained from the 2016 SADHS. Informed consent was obtained from each respondent before the interviews. Procedures and questionnaires for standard DHS surveys have been reviewed and approved by the ICF International Institutional Review Board (IRB). We obtained approval to use the data from the DHS repository (https://​dhsprogram.​com/​data/​available-datasets.​cfm). All methods used in this study were performed in accordance with the Declaration of Helsinki as well as with the relevant guidelines and regulations.
Not applicable.

Competing interests

The authors declare that they have no competing interests.
Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creativecommons.​org/​licenses/​by/​4.​0/​. The Creative Commons Public Domain Dedication waiver (http://​creativecommons.​org/​publicdomain/​zero/​1.​0/​) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Literatur
4.
Zurück zum Zitat Rahimzadeh M, Pourhoseingholi MA, Kavehie B. Survival rates for breast cancer in Iranian patients: a meta-analysis. Asian Pacific J Cancer Prevention: APJCP. 17(4):2223–7. Rahimzadeh M, Pourhoseingholi MA, Kavehie B. Survival rates for breast cancer in Iranian patients: a meta-analysis. Asian Pacific J Cancer Prevention: APJCP. 17(4):2223–7.
6.
Zurück zum Zitat Dolatkhah R, Somi HM, Jafarabadi MA, Hosseinalifam M, Sepahi S, Belalzadeh M, Nezamdoust M, Dastgiri S. Breast Cancer Survival and Incidence: 10 years Cancer Registry Data in the Northwest, Iran. Int. Journal of Breast Cancer 2020; Article ID 1963814, 6 pages. Dolatkhah R, Somi HM, Jafarabadi MA, Hosseinalifam M, Sepahi S, Belalzadeh M, Nezamdoust M, Dastgiri S. Breast Cancer Survival and Incidence: 10 years Cancer Registry Data in the Northwest, Iran. Int. Journal of Breast Cancer 2020; Article ID 1963814, 6 pages.
9.
Zurück zum Zitat World Health Organization (WHO) (2016). The United Nations Global Cervical Cancer Programme End cervical cancer: prevent, treat, care. The Joint Programmes is about catalysing country and global action. The United Nations Inter-Agency Task Force on the Prevention and Control of Non-communicable Diseases (UNIATF). November 2016. WHO/NMH/NMA/16.96 © World Health Organization 2016. World Health Organization (WHO) (2016). The United Nations Global Cervical Cancer Programme End cervical cancer: prevent, treat, care. The Joint Programmes is about catalysing country and global action. The United Nations Inter-Agency Task Force on the Prevention and Control of Non-communicable Diseases (UNIATF). November 2016. WHO/NMH/NMA/16.96 © World Health Organization 2016.
14.
Zurück zum Zitat Ahmed HG, Bensumaidea SH, Alshammari FD, Alenazi F, ALmutlaq BA, Alturkstani MZ, et al. Prevalence of human papillomavirus subtypes 16 and 18 among Yemeni patients with cervical Cancer. Asian Pacific journal of cancer prevention: APJCP. 2017;18(6):1543–8.PubMedPubMedCentral Ahmed HG, Bensumaidea SH, Alshammari FD, Alenazi F, ALmutlaq BA, Alturkstani MZ, et al. Prevalence of human papillomavirus subtypes 16 and 18 among Yemeni patients with cervical Cancer. Asian Pacific journal of cancer prevention: APJCP. 2017;18(6):1543–8.PubMedPubMedCentral
15.
Zurück zum Zitat Chan CK, Aimagambetova G, Ukybassova T, Kongrtay K, Azizan A. Human Papillomavirus Infection and Cervical Cancer: Epidemiology, Screening, and Vaccination—Review of Current Perspectives. Hindawi Journal of Oncology 2019; Article ID 3257939, 11 pages, 1, 11, DOI: https://doi.org/10.1155/2019/3257939. Chan CK, Aimagambetova G, Ukybassova T, Kongrtay K, Azizan A. Human Papillomavirus Infection and Cervical Cancer: Epidemiology, Screening, and Vaccination—Review of Current Perspectives. Hindawi Journal of Oncology 2019; Article ID 3257939, 11 pages, 1, 11, DOI: https://​doi.​org/​10.​1155/​2019/​3257939.
18.
Zurück zum Zitat Akokuwebe ME, Adekanbi DM. Corruption in the health sector and implications for service delivery in Oyo state public hospitals. Ilorin Journal of Sociology. 2017;9(1):200–17. Akokuwebe ME, Adekanbi DM. Corruption in the health sector and implications for service delivery in Oyo state public hospitals. Ilorin Journal of Sociology. 2017;9(1):200–17.
28.
29.
Zurück zum Zitat HPV Center WHO/ICO. HPV Centre WHO/ICO Information Centre on HPV and Cervical Cancer (HPV Information Centre). Human Papillomavirus and Related Cancers in South Africa. Summary Report 2010. Accessed on October 14th, 2020 from https//www.who.in t/hpvcentre. HPV Center WHO/ICO. HPV Centre WHO/ICO Information Centre on HPV and Cervical Cancer (HPV Information Centre). Human Papillomavirus and Related Cancers in South Africa. Summary Report 2010. Accessed on October 14th, 2020 from https//www.​who.​in t/hpvcentre.
32.
Zurück zum Zitat Boyle P, Ngoma T, Sullivan R, Brawley O. Cancer in Africa: the way forward. Special Issue ecancer medical science. 13:953. Boyle P, Ngoma T, Sullivan R, Brawley O. Cancer in Africa: the way forward. Special Issue ecancer medical science. 13:953.
34.
Zurück zum Zitat Morounke SG, Ayorinde JB, Benedict AO, Adedayo FF, Adewale FO, et al. Epidemiology and incidence of common cancers in Nigeria. J Cancer Biol Res. 2017;5(3):1105. Morounke SG, Ayorinde JB, Benedict AO, Adedayo FF, Adewale FO, et al. Epidemiology and incidence of common cancers in Nigeria. J Cancer Biol Res. 2017;5(3):1105.
35.
Zurück zum Zitat Collins SI, Mazloomzadeh S, Winter H, Rollason TP, Blomfield P, Young LS, et al. Proximity of first intercourse to menarche and the risk of human papillomavirus infection: a longitudinal study. Int J Cancer 2005. 2005;114(3):498–500. https://doi.org/10.1002/ijc.20732.CrossRef Collins SI, Mazloomzadeh S, Winter H, Rollason TP, Blomfield P, Young LS, et al. Proximity of first intercourse to menarche and the risk of human papillomavirus infection: a longitudinal study. Int J Cancer 2005. 2005;114(3):498–500. https://​doi.​org/​10.​1002/​ijc.​20732.CrossRef
37.
Zurück zum Zitat National Department of Health (NDOH). National guidelines for cervical cancer screening programme, NDOH, Pretoria, South Africa. National Department of Health. 2000:2000. National Department of Health (NDOH). National guidelines for cervical cancer screening programme, NDOH, Pretoria, South Africa. National Department of Health. 2000:2000.
38.
Zurück zum Zitat Foon S, Bloch B, Mabina M, Carpenter S, Cronje H, et al. Prevalence of pre-cancerous lesions and cervical cancer in South Africa- a multicentre study. S Afr Med J. 2002;92(2):148–56. Foon S, Bloch B, Mabina M, Carpenter S, Cronje H, et al. Prevalence of pre-cancerous lesions and cervical cancer in South Africa- a multicentre study. S Afr Med J. 2002;92(2):148–56.
39.
Zurück zum Zitat Hoque M, Hoque E, Kader SB. Evaluation of cervical Cancer screening program at a rural community of South Africa. East Afr J Public Health. 2008;5(2):111–6.PubMed Hoque M, Hoque E, Kader SB. Evaluation of cervical Cancer screening program at a rural community of South Africa. East Afr J Public Health. 2008;5(2):111–6.PubMed
41.
Zurück zum Zitat Limpopo Department of Health (LDOH). Vote 7 2013/2014 Annual Report 2013/2014 financial year Department of Health 2013/2014. Limpopo Department of Health (LDOH), (2013/2014). Limpopo Department of Health (LDOH). Vote 7 2013/2014 Annual Report 2013/2014 financial year Department of Health 2013/2014. Limpopo Department of Health (LDOH), (2013/2014).
42.
Zurück zum Zitat Arulogun OS, Maxwell OO. Perception and utilization of cervical cancer screening services among female nurses in university college hospital, Ibadan. Nigeria Pan Afr Med J. 2012;11(1):69.PubMed Arulogun OS, Maxwell OO. Perception and utilization of cervical cancer screening services among female nurses in university college hospital, Ibadan. Nigeria Pan Afr Med J. 2012;11(1):69.PubMed
43.
Zurück zum Zitat Lim JN, Ojo AA. Barriers to utilisation of cervical cancer screening in sub-Saharan Africa: a systematic review. Eur J Cancer Care (Engl). 2017;26(1):1–9.CrossRef Lim JN, Ojo AA. Barriers to utilisation of cervical cancer screening in sub-Saharan Africa: a systematic review. Eur J Cancer Care (Engl). 2017;26(1):1–9.CrossRef
49.
Zurück zum Zitat Statistics South Africa General Household Survey 2017. Statistics South Africa 2018. Statistics South Africa General Household Survey 2017. Statistics South Africa 2018.
50.
Zurück zum Zitat World Bank. Overcoming poverty and inequality in South Africa: an assessment of drivers, constraints, and opportunities. 2018:148. World Bank. Overcoming poverty and inequality in South Africa: an assessment of drivers, constraints, and opportunities. 2018:148.
51.
Zurück zum Zitat South Africa Demographic and Health Survey (SADHS), 2016. National Department of Health (NDoH), Statistics South Africa (Stats SA), South African Medical Research Council (SAMRC), and ICF. 2017. South Africa Demographic and health survey 2016: key indicators. Pretoria, South Africa, and Rockville, Maryland, USA: NDoH, Stats SA, SAMRC, and ICF. South Africa Demographic and Health Survey (SADHS), 2016. National Department of Health (NDoH), Statistics South Africa (Stats SA), South African Medical Research Council (SAMRC), and ICF. 2017. South Africa Demographic and health survey 2016: key indicators. Pretoria, South Africa, and Rockville, Maryland, USA: NDoH, Stats SA, SAMRC, and ICF.
52.
Zurück zum Zitat Iqbal J, Ginsburg O, Rochon PA, Sun P, Narod SA. Differences in breast cancer stage at diagnosis and cancer-specific survival by race and ethnicity in the United States. JAMA. 313(2):165–73. Iqbal J, Ginsburg O, Rochon PA, Sun P, Narod SA. Differences in breast cancer stage at diagnosis and cancer-specific survival by race and ethnicity in the United States. JAMA. 313(2):165–73.
59.
Zurück zum Zitat Somdyala NIM, Bradshaw D, Dhansay MA, Stefan DC. Increasing cervical cancer incidence in rural Eastern Cape Province of South Africa from 1998 to 2012: A population-based cancer registry study. JCO Glob Oncol. 2020; 6: JGO. 19.00198. Somdyala NIM, Bradshaw D, Dhansay MA, Stefan DC. Increasing cervical cancer incidence in rural Eastern Cape Province of South Africa from 1998 to 2012: A population-based cancer registry study. JCO Glob Oncol. 2020; 6: JGO. 19.00198.
60.
Zurück zum Zitat Agarwal S, Ying J, Boucher KM, Agarwal JP. The association between socioeconomic factors and breast cancer-specific survival varies by race. PLoS One. 2017;12(12):Article e0187018.CrossRef Agarwal S, Ying J, Boucher KM, Agarwal JP. The association between socioeconomic factors and breast cancer-specific survival varies by race. PLoS One. 2017;12(12):Article e0187018.CrossRef
66.
Zurück zum Zitat de Sanjose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect. Dis. 2017;7:453–453–9. de Sanjose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect. Dis. 2017;7:453–453–9.
69.
Zurück zum Zitat Akokuwebe ME, Okafor EE. Maternal health and the implications for sustainable transformation in Nigeria. Res Humanit Soc Sci. 2015;5(6):1–3. Akokuwebe ME, Okafor EE. Maternal health and the implications for sustainable transformation in Nigeria. Res Humanit Soc Sci. 2015;5(6):1–3.
71.
Zurück zum Zitat Idowu A, Olowookere SA, Fagbemi AT, Ogunlaja OA. Determinants of cervical cancer screening uptake among women in Ilorin, North Central Nigeria: A community-based study. J Cancer Epidemiology 2016; Article ID 6469240, 8 pages. Idowu A, Olowookere SA, Fagbemi AT, Ogunlaja OA. Determinants of cervical cancer screening uptake among women in Ilorin, North Central Nigeria: A community-based study. J Cancer Epidemiology 2016; Article ID 6469240, 8 pages.
73.
Zurück zum Zitat Tiruneh FN, Chuang K-Y, PAM N, Chuang Y-C. Individual-level and community-level determinants of cervical cancer screening among Kenyan women: a multilevel analysis of a nationwide survey. BMC Women’s Health. 2012;17:109.CrossRef Tiruneh FN, Chuang K-Y, PAM N, Chuang Y-C. Individual-level and community-level determinants of cervical cancer screening among Kenyan women: a multilevel analysis of a nationwide survey. BMC Women’s Health. 2012;17:109.CrossRef
77.
Zurück zum Zitat Bruni L, Albero G, Serrano B, Mena M., Gomez D, Munoz J, Bosch FX, de Sanjose S. ICO/IARC Information Centre on HPV and cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in Namibia. Summary Report 17 June 2019. [Accessed on July 27th, 2021]. Bruni L, Albero G, Serrano B, Mena M., Gomez D, Munoz J, Bosch FX, de Sanjose S. ICO/IARC Information Centre on HPV and cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in Namibia. Summary Report 17 June 2019. [Accessed on July 27th, 2021].
Metadaten
Titel
Determinants and levels of cervical Cancer screening uptake among women of reproductive age in South Africa: evidence from South Africa Demographic and health survey data, 2016
verfasst von
Monica Ewomazino Akokuwebe
Erhabor Sunday Idemudia
Abiel M. Lekulo
Ogone Warona Motlogeloa
Publikationsdatum
01.12.2021
Verlag
BioMed Central
Erschienen in
BMC Public Health / Ausgabe 1/2021
Elektronische ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-021-12020-z

Weitere Artikel der Ausgabe 1/2021

BMC Public Health 1/2021 Zur Ausgabe