Abbreviations:

Pap smear: Papanicolaou smear; VIA: Visual inspection by acetic acid; FGM: Female genital mutilation; WHO: World health organization

1. Introduction

Globally, cervical cancer constitutes the second common type of cancer among women, with an annual 500,000 new cases and 274,000 deaths [1]. In developing countries, it constitutes the commonest cancer affecting women [1] with 85% of the total numbers of cases worldwide [2]. In Sudan, approximately 833 females get diagnosed annually with cervical cancer, with an annual incidence and deaths of 7.9 per 100,000 and 534 respectively [3]. Human Papilloma virus (HPV)constitutes a primary cause of cervical cancer, along with other sexually transmitted infections like Chlamydia Trachomatis [4]. Other risk factors include multiple sexual partners, early age of sexual activity, 5 years or more usage of hormonal contraceptive, smoking, alcohol consumption and specific diet [5-9].

Cervical cancer is a preventable disease that can be detected in early stages -as pre-cancerous lesions- by screening tests like Papanicolaou (Pap) smear and visual inspection by acetic acid (VIA) [10]. In developed countries, treatment of pre-cancerous lesions at the early stages of cervical cancer prevents 80% of cases [1]. In contrast, screening programs are less implementable in countries with low source settings, weak health systems with a lack of well-trained health professionals and a low level of awareness about the disease, which leads to an increased cervical cancer mortality rate in such developing countries [1, 11]. This study aimed to assess the knowledge, attitude and practice of Sudanese women towards cervical cancer and its screening tests “Pap smear and VIA” in Saad Abu El Ella teaching hospital, Khartoum-Sudan.

2. Materials and Methods

2.1 Study design

This is an observational cross-sectional hospital-based study.

2.2 Study setting

The study was conducted in Saad Abu El Ella teaching hospital which is a public hospital affiliated with Khartoum university and located in Khartoum city. Data were collected from 12 to 30 August 2020 using an anonymous self-administered questionnaire which was developed from previous studies [11, 12] and also by a senior obstetrician and gynaecologist. It was translated into Arabic and has items about demographics, obstetrics and gynaecological history, knowledge, attitude and practice towards cervical cancer and Pap smear/VIA.

2.3 Study participants

Inclusion criteria were: all women who attended the outpatient clinics and wards, aged between 18 to 65 years. Exclusion criteria were: women who were non-Arabic speakers, younger than 18 years or refused to participate. Women had been selected randomly from clinics and wards.

2.4 Variables

The outcomes in multiple linear regression were scores of knowledge, attitude and practice, and the predictors were items of demographics, obstetrics and gynaecological history and scores of knowledge, attitude and practice about cervical cancer and its screening tests. The potential confounders -not shown in the manuscript- were those variables with P values more than 0.1 in univariable unadjusted linear regression.

2.5 Data sources/measurement

The classification method of the predictors and outcome was based on a previous study [12] and also based on the instructions of the supervisor (senior obstetrician and gynaecologist).

2.6 Bias

To address information bias, each questionnaire had been revised immediately after being filled up to correct misunderstandings, i.e. to avoid socially acceptable answers rather than the truth. Linear regression was used to address confounding bias where variables in the univariable unadjusted linear regression with P values more than 0.1 were considered as confounding variables and then were removed from the final multivariable linear regression model. Since the sampling technique was convenient, no attempts had been done to address selection bias.

2.7 Study size

The sample size was 310 which was collected conveni-

ently through total coverage of women who attended the clinics and wards in the period between 12 to 30 August 2020.

2.8 Quantitative variables

The continuous variables had been grouped based on the instructions of the supervisor. Participants' monthly income was categorized into low, moderate and high-income categories [13]. Knowledge score was calculated based on 12 items out of 15, while attitude and practice scores both had been calculated based on 2 items for each of them. The scores were calculated as follows: each correct answer had a score of 2, each incorrect answer had a score of zero and answers of “I do not know” had a score of one. The total knowledge score was 46 and classified as poor (0-15), moderate (16-25) and good (35-46), while the total attitude and practice scores were 4 of each of them and classified as poor (0-2) and good (3-4).

2.9 Statistical methods

Data were coded and analyzed using Statistical Package for the Social Sciences (SPSS) version 23, both descriptive and inferential statistics were performed. Analysis of variance (ANOVA) and independent-samples T-test was used to compare the statistical differences of scores between different groups. Spearman rho correlation was used to assess the relationship between the scores. Univariable unadjusted linear regression was performed between demographics, obstetrics and gynaecological history and scores of knowledge, attitude and practice, and the scores as outcomes.

Variables in the univariable unadjusted linear regression with P values less than 0.1 were considered as potential risk factors and then included in multivariable-adjusted linear regression. The missing data were excluded using the option “exclude cases pairwise” in SPSS. Data are presented using frequency tables. The type of per cent that are mentioned in the text is the “actual Percent” not the “Valid per cent”.

2.10 Ethical approval

The study was approved by the ethical committee of the department of community medicine-university of Khartoum. Also, permission was taken from the administration of Saad Abu El Ella teaching hospital. Informed verbal consents had been taken from all of the respondents.

3. Results

3.1 Demographics

A total of 310 women participated in this study. The mean age was 32 years (± 9SD “standard deviation”), and the majority belonged to the age group 20-30 years (45.5%, 141/310). 90.0% of the participants were Muslims (307/310) and most of them (44.8%, 139/310) had Bachelor degree. Furthermore, half of them worked as housewives (46.1%, 143/310) and 86.8% (269/310) of them were married (sexually active).The mean monthly income was 87.9U.S. dollars (± 159.3 SD), and the majority of the respondents had low income (37.4%, 116/310). Table1.

3.2 Obstetrics and gynecological history

About 35.8% (111/310) of the respondents used contraceptives and 43.5% (135/310) of them had health insurance. 27.7% (86/310) of the participants had undergone vaginal speculum examination and 20.3% (63/310) complained about it as a painful procedure. 80.0% (248/310) of the participants underwent FGM [1]. According to WHO [2], FGM has four types(World Health Organization, 2020). Most of the FGMs reported in this study were WHO type 3 (38.1%, 118/310) Table 1.

3.3 Knowledge about cervical cancer and its screening tests

Halfof the respondents (50.0%, 155/310) heard about cervical cancer. The most reported symptoms in this study were: abnormal vaginal bleeding between periods (35.8%, 111/310) and malodorous vaginal discharge (28.1%, 87/310). While the most frequently risk factors were: smoking (30.0%, 93/310), sexually transmitted infections (30.0%, 93/310), multiple partners (28.7%, 89/310) and poor personal hygiene (25.8%, 80/310). Other symptoms and risk factors are mentioned in table 2 and table 3 respectively. Around 21.3% (66/310) of women in this study knew that a virus (HPV: human Papilloma virus) can cause cervical cancer. Moreover, 14.5% (45/310) them knew that HPV virus is sexually transmitted. Likewise, only 9.4% (29/310) of them knew about the vaccine against that virus. About 27.7% (86/310) of the respondents heard about Pap smear and visual inspection of the cervix with acetic acid (VIA), mainly from media(television, radio and internet) (13.5%, 42/310). 9.7% (30/310) of the participants mentioned that these tests are performed using speculum and 7.7% (24/310) of them mentioned that postmenopausal women are recommended for Pap smear/VIA. The mean total knowledge score was 12.4 (± 13.1 SD). Most of the respondents had poor knowledge (54.5%, 169/310). Table 4 shows other information regarding knowledge about cervical cancer and its screening tests.

3.4 Attitude and practice towards Pap smear and VIA

Around 65.2% (202/310) of the respondents agreedto perform Pap smear and VIA. While 23.5% (73/310) of them refused to perform these screening tests due to the following reasons: “might be painful” (16.8%, 52/310), “not interested” (16.8%, 52/310) and “I am healthy, no need” (13.2%, 41/310). Other reasons of refusal to perform these screening tests are mentioned in table 5. The majority of the participants 85.5% (265/310) agreed to participate in educational campaigns about cervical cancer and its screening tests. The mean total attitude score was 3 (± 1.3 SD). Most of the respondents had good attitude (61.3%, 190/310). Only 2.3% (7/310) of the respondents had ever undergone screening tests for cervical cancer (Pap smear/VIA). Also, only 2.3% (7/310) of them have ever received vaccine for human Papilloma virus. The mean total practice score was 0.09 (± 0.41 SD). All of the respondents had poor practice (100.0%, 310/310). One-way between-groups ANOVA was conducted to explore the impact of educational level and occupation on knowledge score. Post-hoc comparisons using the Tukey HSD test indicated that the mean knowledge score for postgraduates (mean 17.5, SD 14.2) was significantly different from secondary school students (mean 10.6, SD 12.6) and university students (mean 11.2, SD 12.4). Also, it indicated that the mean knowledge score for housewives (mean 9.3, SD 11.7) was significantly different from employees (mean 14.4, SD 13.2) freelancers (mean 22, SD 12.9).

An independent-samples t-test was conducted to compare practice score for women who had used contraceptives and those who had not. There was significant difference in practice scores for those who had used contraceptives (mean 0.14, SD 0.52) and those who had not (mean 0.05, SD 0.3). The relationship between knowledge score and attitude and practice scores was investigated using Spearman rho correlation. There were weak positive, correlations between knowledge and attitude scores, r = 0.16, n = 310, P value = 0.004, and also between knowledge and practice scores, r = 0.17, n = 310, P value = 0.002. With high levels of knowledge score associated with high levels of attitude and practice scores. A multiple linear regression was calculated to predict knowledge score based on: age, educational level, occupation, contraceptives usage and history of vaginal speculum examination. The full model was statistically significant, P value = 0.000, R² =0.15. Knowledge score decreases by 0.12 for each year of age, decreases by 0.15 for being housewife, and increased by 0.15 for using contraceptives Table 6.

A multiple linear regression was calculated to predict attitude score based on: educational level, occupation and knowledge score. The full model was statistically significant, P value = 0.000, R² = 0.103. Attitude score increases by 0.21 for being postgraduates, increases by 0.17 for each score of knowledge, and decreases by 0.19 for being a housewife Table 7. A multiple linear regression was calculated to predict practice score based on: educational level, contraceptives’ usage and knowledge score. The full model was statistically significant, P value = 0.001, R² = 0.082. Practice score decreases by 0.77 for being university students and increases by 0.14 for each score of knowledge Table 8.

Table 1: Demographics and obstetrics/gynecological history (n 310).

Table 2: Symptoms of cervical cancer (n 310).

Table 3: Risk factors of cervical cancer (n 310).

Table 4: Items of knowledge about cervical cancer and its screening tests (n 310).

Table 5: Reasons of refusal to perform Pap smear/VIA (n 310).

* CI: confidence interval. R² adjusted = 0.15

Table 6: Multiple linear regression for predictors of knowledge score.

* CI: confidence interval. R² adjusted = 0.103

Table 7: Multiple linear regression for predictors of attitude score.

* CI: confidence interval. R² adjusted = 0.082

Table 8: Multiple linear regression for predictors of practice score.

4. Discussion

Half of the respondents (50.0%, 155/310) in this study heard about cervical cancer and 27.7% (86/310) of them heard about Pap smear/VIA. The majority of the respondents (65.2%, 202/310) agreed to perform Pap smear and VIA, and 85.5% (265/310) of them agreed to participate in educational campaigns to teach other women about cervical cancer and its screening tests. Only the minorities of our participants had ever undergone Pap smear/VIA (2.3%, 7/310) and received the vaccine against the Human Papillomavirus (2.3%, 7/310). About 50.0% (155/310) and 27.7% (86/310) of women in our study heard about cervical cancer and Pap smear/VIA, respectively. In fact, most of those who mentioned that they “heard about cervical cancer” had limited knowledge as evidenced by the fact that considerable percentages of them -shown in table 2 and 3- didnotrate the followings as symptoms and risk factors of cervical cancer: increased vaginal discharge (52.9%, 82/155), dyspareunia (43.4%, 67/155), sexually transmitted infections (34.2%, 53/155), smoking(34.2%, 53/155)and low socioeconomic status (55.5%, 86/310), as they were less likely to undergo cervical cancer screening tests. Also -out of those who heard about cervical cancer- 47.7% (74/310) did not rate HPV as a risk factor of cervical cancer. This finding is accordant with a Cameroonian study in which 76.6% of the respondents were ignorant about HPV as a risk factor for cervical cancer [14].

Out of those participants who mentioned that they “heard about Pap smear/VIA” in this study: 52.3% (45/86) of them thought that it is unnecessary to repeat these tests during life. The previous findings reflected their poor awareness about cervical cancer and Pap smear/VIA, which is accordant with a study conducted in Malaysia which indicated that many of the respondents did not rate the following as symptoms and risk factors of cervical cancer: malodorous vaginal discharge, abnormal vaginal bleeding between menstruation, dyspareunia, HPV and HIV infections, multiple partners, early age at marriage and smoking [12].Still high, the percentage of our participants who hadneverheard about cervical cancer (47.4%, 148/310) and Pap smear/VIA (70.3%, 218/310) as a study conducted in Ghana and indicated that: 68.4% and 97.7% of the respondents had never heard about cervical cancer and Pap smear respectively, and only5.9% of them knew about sexual transmission of HPV [15]. Unawareness about sexual transmission of HPV as a primary cause of cervical cancer can lead to disease multi-spread, especially with multiple partners as indicated in the study [15] that lacking knowledge about sexual transmission of HPV can lead women to be infected with the virus without being aware of the source of infection. Poor level of knowledge about cervical cancer and its screening tests could be explained by knowing that many of the respondents had limited education and low economic status that prevented them from having access to cervical cancer screening tests. Limited knowledge about cervical cancer constitutes a barrier against having periodic Pap smear/VIA tests, this may implicate on women being presented in advanced stages of the disease [15]. Previous studies indicated that well-educated women were more likely to be aware of cervical cancer and Pap smear [11, 16]. Likewise, low educational level was associated with low awareness of cervical cancer [16].

In this study, 65.2% (202/310) of the respondents had the desire to undergo Pap smear/VIA test, mainly represented by those who had good and moderate knowledge scores and had high education, which reflects the importance of education in the prevention of cervical cancer. This result is accordant with a Cambodian study that indicated 74.0% of the participants had the desire to undergo a Pap smear, despite their low level of knowledge about cervical cancer and its prevention [17]. Authorities should encourage Pap smear/VIA testing by providing them opportunistically -during clinics’ visits- and voluntary. As shown in Table 4, the highly-rated reasons for refusal of Pap smear/VIA were: “painful”, “unnecessary” and “I am healthy, no need”. likewise, previous studies indicated pain and non-necessity as the major reasons for the refusal [11, 12]. While another previous study [12] indicated that religious factors can negatively affect the attitude towards Pap smear, as the respondents had to gain consent from their spouses. Furthermore, in this study 20.3% (63/310) of the respondents had a painful vaginal examination, and 80.0% (248/310) had had FGM, commonly WHO type 3 was (38.1%, 118/310). So painful experiences and embarrassment with genitalia have been shown to negatively affect cervical cancer screening tests [18]. Fortunately, most of the respondents (85.5%, 265/310) had the desire to educate other women about cervical cancer and its screening tests through participation in educational campaigns. Most of them had Bachelor degrees and had moderate and good knowledge scores, which could reflect the effect of education and awareness about cervical cancer in attitude level towards cervical cancer.

In this study, the rate of Pap smear/VIA testing was low (2.3%, 7/310), which represented mainly the respondents who: used contraceptives (85.7%, 6/7), underwent FGM (100.0%, 7/7) and had vaginal speculum examination (42.9%, 3/7). This result is accordant with a study conducted in Sudan which indicated that only 15.8% of women had ever undergone Pap smear/VIA, and that percentage has mainly represented those women with: Bachelor degrees, urban-living, age more than 30 years and a history of gynaecological examination [11]. This low testing rate can be explained by socio-demographics: the majority of our participants were relatively young and had low economic status. Young women find themselves healthy and less likely to seek medical care. Moreover, a considerable percentage ofthe participants had never been to university, and only 27.7% (86/310) heard about Pap smear/VIA.Since the developed countries have high-income status, so it is expected to have high percentages of cervical cancer screening tests there as a study conducted in the United States of America (USA) indicated that 93.0% of the American women had undergone at least one Pap smear in their lifetime [19].There was a significant difference in practice scores-as reflected by having Pap smear/VIA and HPV vaccine- between those who had used contraceptives and those who had not. This can be explained by knowing that most contraceptives’ users were well educated.

Only 2.3%(7/310) of the participants received the HPV vaccine and mainly represented by those with moderate and good knowledge of cervical cancer. A Cambodian study indicated that only 1.0% had received the HPV vaccine, and the major reasons for refusal of the HPV vaccine included poor knowledge about it and its high cost [17]. Therefore, to increase HPV vaccination coverage, it is crucial to decrease its cost by providing the women with health insurance and increase their awareness about the importance of this vaccine through different channels (media, educational campaigns and opportunistic education during clinics’ visits). We found that having contraceptives and higher knowledge score were positively associated with practice score, which is accordant with a study that indicated that women who used contraceptives were 3.97 times more likely to undergo Pap smear than those who did not use contraceptives, and women with higher knowledge score were 1.09 times more likely to undergo Pap smear than those without higher knowledge score [12]. The study has limitations. Since the study design is cross-sectional, it limits the establishment of cause and effect relationship between predictors and outcome. Unmeasured, residual and imprecisely measured confounders might affect the regression model. Since some women were non-Arabic speakers, the language barrier was an issue.

5. Conclusions

Although most of the respondents had heard about cervical cancer and its screening tests, most of the respondents had limited knowledge about cervical cancer and its screening tests, which reflects the importance of implementing health educational campaigns. Also, most of them had undergone neither Pap smear/VIA nor HPV vaccine before. As most of them had the desire to undergo Pap smear/VIA, these tests should be implemented through primary health care centres.

Recommendations

The results of the study should be reported to the health stakeholders in order to direct them into conducting health educational campaigns about cervical cancer and to implement feasible and cost-effective screening programs. Rural areas should be reached through mobile teams. Community participation in health education campaigns should be encouraged to increase the level of awareness, attitude and practice towards the disease. Also, vaccination programs against HPV should be implemented.

Acknowledgements

We sincerely acknowledge all the women who participated in this study and those who guided me to finish this manuscript. No institute has funded this study.

Competing Interest

None declared.

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