Annals of African Medicine

: 2021  |  Volume : 20  |  Issue : 3  |  Page : 212--221

Cervical cytopathological changes in pregnancy: An experience from a low resource setting

Fatima Abubakar Rasheed1, Ibrahim Adamu Yakasai2, Idris Usman Takai2, Ibrahim Yusuf3, Usman Muhammad Ibrahim4,  
1 Department of Obstetrics and Gynaecology, Federal Medical Centre, Katsina, Nigeria
2 Department of Obstetrics and Gynaecology, Bayero University, Kano/Aminu Kano Teaching Hospital, Kano, Nigeria
3 Department of Histopathology, Bayero University, Kano/Aminu Kano Teaching Hospital, Kano, Nigeria
4 Department of Community Medicine, Aminu Kano Teaching Hospital, Kano, Nigeria

Correspondence Address:
Dr. Idris Usman Takai
Department of Obstetrics and Gynaecology, Bayero University, Kano/Aminu Kano Teaching Hospital, PMB 3011, Kano


Background: Cervical cancer is the leading cause of death among women in developing countries. It is preventable through effective cervical cancer screening program. However, in Nigeria, screening programs are opportunistic and coverage is insufficient to make an impact. Aim: This study assessed the cervical cytopathological changes among pregnant women at booking using liquid-based cytology (LBC) in Aminu Kano Teaching Hospital (AKTH). Methodology: This was a cross-sectional study that was carried out at the antenatal Clinic of AKTH, Kano, Nigeria. A total of 161 pregnant women who fulfilled the criteria and gave their consent were recruited into the study using systematic sampling technique at booking for antenatal care. LBC was employed using standard procedure and samples sent to histopathology department for analysis. Pro forma developed for the study was used to obtain the socio-demographic and reproductive characteristics of the women and the risk factors for abnormal cervical cytology. Results: Out of the 161 pregnant women that had cervical cytology screening using LBC on their first prenatal visit during the study, 22 had abnormal cervical cytology, giving a prevalence rate of 13.7%. Out of this, six (27.3%) were atypical squamous cells of undetermined significance, 3 (13.6%) were Atypical Squamous Cells, Cannot Rule Out HSIL (ASC-H), 11 (50.0%) were low-grade Squamous Intraepithelial Lesions while 2 (9.1%) were high grade squamous intraepithelial lesions. Negative smears were seen in 104 women (64.6%). Inflammatory and other conditions of the cervix which are technically negative smears made up the remaining 21.7%. There was a statistically significant association between cervical cytology results and advanced age (P < 0.01), increasing number of lifetime sexual partners since coitarche (P < 0.01), high parity (P < 0.01), absent previous Pap test (P < 0.027), previous history of sexually transmitted infections (P < 0.040), and positive HIV status (P < 0.001). Following binary logistic regression, advanced maternal age, increasing number of sexual partners, high parity, and positive HIV status stood out to be independent predictors of premalignant lesions of the cervix in pregnancy in this study. Conclusion: Advanced maternal age, increasing number of sexual partners, high parity, and positive HIV status stood out to be independent predictors of premalignant lesions of the cervix in the study. Routine cervical cytology screening using LBC should be offered to all antenatal clients in our setting to increase coverage and detection rate of preinvasive lesions of the cervix, and/or pregnant women with increased risk of abnormal cervical cytology from this study.

How to cite this article:
Rasheed FA, Yakasai IA, Takai IU, Yusuf I, Ibrahim UM. Cervical cytopathological changes in pregnancy: An experience from a low resource setting.Ann Afr Med 2021;20:212-221

How to cite this URL:
Rasheed FA, Yakasai IA, Takai IU, Yusuf I, Ibrahim UM. Cervical cytopathological changes in pregnancy: An experience from a low resource setting. Ann Afr Med [serial online] 2021 [cited 2022 Jan 18 ];20:212-221
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Full Text


Carcinoma of the cervix is the second most common cancer among women worldwide, and the seventh overall,[1],[2],[3] and is the leading cause of cancer death among women in developing countries.[2],[4],[5] Luckily, it is preventable, because it has a well-defined premalignant phase,[6] and in countries where cervical cancer screening programs are efficient, the prevalence of invasive cancer of the cervix is very low, like in Sao Paulo, South America where 0.2% was reported.[7]

The precancerous lesions usually begin with infection of the metaplastic epithelium of the transformation zone of the cervix with one or more of the high-risk oncogenic human papillomavirus (HPV),[6],[7] the invasive spectrum develops only when there is persistent HPV-DNA in the cells.[8],[9] Up to 99.7% of cervical cancers worldwide contains HPV DNA.[10] Worldwide, approximately 291 million women (10.4%) have cervical HPV infection at a point in time,[1] which makes timely vaccination with HPV vaccine an effective primary prevention method. However, the cost and availability makes it inaccessible in developing countries, thereby leaving secondary prevention through cervical cytology screening as the best available option of cervical cancer prevention as at now in developing countries like Nigeria.[3]

Carcinoma of the cervix is a significant global health burden,[11] most common cancer among women in Sub-Saharan Africa,[12],[13] and the leading cause of cancer death in underdeveloped world.[14],[15] In Nigeria, cervical cancer is the most common malignancy of the female genital tract.[16],[17] Annually, about 40 million Nigerian women are at risk of developing cervical cancer which has a national age-standardized incidence of 33.0/100000 women per year.[18],[19] Every year approximately 14,089 new cervical cancer cases are diagnosed in Nigeria and 8,240 women die from the disease.[19]

Cervical cancer accounts for 62.3%–70.5% of all gynecological cancers in Kano,[13],[20] and is the most common gynecological cancer at Aminu Kano Teaching Hospital (AKTH), constituting 48.6% followed by ovarian cancer with 30.5%.[13] The commonest histological type of cervical cancer is squamous accounting for 35.42% of all malignancies in AKTH, with majority presenting in the late stage.[21] Nigeria like other developing countries, lacks a well-implemented national cervical cancer screening policy.[22],[23] Screening for cervical cancer is mainly opportunistic,[24],[25] making screening coverage insufficient to have an impact,[26] with only 8.7% of women above the ages of 18 years ever been screened.[18],[19]

One method that can increase coverage is the integration of cervical cytology screening into an existing and popular women's health programs such as routine antenatal care (ANC) – the canopy program that delivers a range of health services to women in pregnancy.[27] The prevalence of ANC visits ranges from 84.6% in Nigeria to 97% in Tanzania.[28] There is also evidence that women attending ANC demonstrate a strong enthusiasm to adhere to medical follow-up and care instructions throughout the course of pregnancy.[27] Currently, a new approach to cervical cytology, in which cells collected in liquid preservatives are used to prepare slides for staining, has been developed in an effort to produce more demonstrative cytological preparations with fewer artifacts.[29] Evidence-based studies have shown liquid based cytology (LBC) offers some weighty advantages over conventional Pap smear since it requires fewer test and fewer visits to the clinic.[30]

There is paucity of data on cervical cancer screening in pregnancy from Kano, and none that utilize LBC as screening method from Northern Nigeria. This study therefore evaluated the pattern of cyto pathological changes of the cervix and identified the prevalence of abnormal cervical cytology amongst pregnant women at booking using LBC in AKTH, Kano. Findings from this study, may lead to a change in the existing screening protocol in our hospital and Kano at large, as it may help to ensure that we do not miss detection of cases in women that are lost to follow-up during the postpartum period, and as part of a strategic framework in curtailing high incidence of cervical cancer and the mortality from this preventable cause of death among our women.


The study was conducted at the antenatal clinic of Obstetrics and Gynecology Department of AKTH.[31],[32],[33] Descriptive cross-sectional design was used to study all pregnant women before 28 weeks of gestation attending the antenatal clinic for their booking visit. Pregnant women aged 25 years and above were included while pregnant woman who were bleeding at the time of contact, those with history of threatened miscarriage in the current pregnancy, history of preterm labor in previous pregnancy, those at booking who have had her cervical screening within the past 2 years and it was normal and pregnant women with visible cervical lesion on speculum examination were excluded from the study. A sample of 161 was determined using Taylor's formula for proportion for estimating minimum sample size for descriptive studies,[34] using point prevalence of 10% from the previous study[35] and possible nonresponse rate of 10%.

Systematic sampling technique was used to study the eligible patients. Sampling interval of 2 was obtained as the ratio of sample frame (240 that is average number of ANC bookings per month) to sample size (161). The first respondent was obtained by simple balloting using numbers from 1 to 2 from which 2 was randomly selected. Therefore, the second respondent was the first to be studied. Subsequent respondents were obtained by adding the sampling interval until the calculated sample size was obtained.

Recruitment was done on all antenatal clinic days. Three senior registrars from the department of obstetrics and gynecology were trained for the study. Brief screening questions were obtained from each woman to exclude all possible exclusion criteria before she is being recruited for the study. A written informed consent was obtained from those willing to participate after going through the consent form with them in details.

A proforma developed for the study was used to obtain information on the socio-demographic characteristics of the respondents and the risk factors for abnormal cervical cytology and recorded on the pro forma. Speculum examination findings were also recorded. Women first received the routine booking care package that every woman at first prenatal visit receives, in addition to the administration of proforma and the cervical cytology smear. LBC technique was employed. Before the procedure, each participant was provided with additional information and counseling. The women were asked to void if they had the urge to. Following exposure and visualization of the ectocervix and squamocolumnar junction, systematic inspection of the vaginal fornices and cervix was done and findings noted were recorded. Specimens for microscopy were taken from women with profuse vaginal discharge for microcopy, culture and sensitivity. Results were reported according to the Bethesda system.[36] Patients with infections and those who had abnormal results were counseled, reassured, and managed appropriately.

The thin prep system for Pap specimen was based on FDA guideline.[37] Processing started in the laboratory by mixing the specimen well and pouring it into a 15 ml centrifuge tube and Papanicolaou staining technique was used for analysis and a trained cytopathologist interpreted all the slides (As in [Figure 1], [Figure 2], [Figure 3]a & [Figure 3]b, [Figure 4] and [Figure 5].{Figure 1}{Figure 2}{Figure 3}{Figure 4}{Figure 5}

Data obtained from the proforma was entered into Microsoft Excel sheet and subsequently checked for errors and inconsistencies. SPSS version 23 computer software SPSS statistical package version 23 (SPSS.23 Inc, Chicago, USA, 2016) was used to analyze the data. Qualitative variables were summarized as frequencies and percentages, quantitative variables were summarized as means and standard deviations were appropriate. The outcome variable was cervical cytology status while the independent variables were the socio-demographic characteristics. Person's Chi-square/Fisher's exact test or t-test was used where appropriate to determine association between categorical or numerical variables respectively and P ≤ 0.05 was considered statistically significant. Factors found to be significantly associated with abnormal cervical cytology on bivariate analysis were included in the logistic regression model to control for confounding variables.

Ethical approval was obtained from the Research and Ethics Committee of AKTH with approval number NHREC/21/08/2008/AKTH/EC/2277, dated 19/07/2018. Data was collected from October to December, 2018. The provisions of the Helsinki Declaration (2013) on investigation of human subjects were adhered to throughout the study and the cost of the research was entirely bored by the researcher.


Socio-demographic and reproductive characteristics of pregnant women

[Table 1] summarizes the socio-demographic and reproductive profile of the pregnant women. The mean age of the women in this study was 30.7 ± 4.85 years, with a range of 18–42 years. Most (82%) were within the age range 25–34 years. Eighty-four point five percent (136) of the women were Hausa/Fulani by tribe, other tribes included Igbo, Yoruba, Nupe and Igbira as shown in the table. A great majority 149 (92.5%) of the women belonged to the Islamic faith. Up to 50.3% of the women in the study had education up to tertiary level; only 5 (3.1%) reported no formal education. Although about half had tertiary education, 83 (51.6%) were unemployed, 42 (26.1%) were self-employed and only 36 (22.4%) were civil-servants. Almost all (97.5%) were married. Among those who were married, 115 (71.4%) were in a monogamous family setting and in their first order of marriage 144 (89.4%). Forty-one (25.5%) were grand multiparous women. The mean gestational age at booking was found to be 23.1 ± 4.23 weeks. About 29 (18.0%) presented for their first prenatal visit after the second trimester, only 5 (3.1%) presented in the 1st trimester.{Table 1}

Prevalence of abnormal cervical cytopathology among pregnant women at booking

Twenty-two women tested positive for premalignant lesions, giving a prevalence of abnormal cervical cytology of 13.7%, as depicted in [Table 2].{Table 2}

Pattern of cytopathological changes of the cervix among pregnant women

[Table 3] shows the pattern of cytopathological changes of the cervix amongst pregnant women at booking. Among those that tested positive for abnormal cervical cytology, low-grade Squamous Intraepithelial Lesions (LSIL) was the predominant form seen in 11 (50%) of the pregnant women, while high-grade squamous intraepithelial lesions (HSIL) was seen in 2 (9.1%). Up to 104 (64.6%) tested negative for intraepithelial lesion or malignancy while inflammatory changes were present among 35 (21.7%) of the study population.{Table 3}

Factors associated with cervical cytopathological reports at booking

[Table 4] shows the relationship between cervical cyto-pathological reports at booking with some possible associated factors among the study population. There was statistically significant difference in the mean age of the women across the two groups, with abnormal cervical cytology having a higher mean age (t = 3.37, P ≤ 0.01). Mean number of sexual partners also showed a significant difference across the two groups (t = 4.879, P ≤ 0.01). Age at coitarche however, did not show any statistical difference (t = −0.813, P = 0.417). HIV status (fishers exact, P = 0.001) and parity (χ2 = 17.752, P ≤ 0.01) were significantly associated with abnormal cervical cytology. Educational status, marital status, and social class on the other hand were not significantly associated with cervical cytological findings.{Table 4}

Predictors of cervical cytology abnormalities

Logistic regression analysis was conducted to rule out potential cofounders. Advancing maternal age (P < 0.035), high parity (P < 0.01), positive HIV status (P < 0.001), and number of lifetime sexual partners (P < 0.01) were independent predictors of abnormal cervical cytology. The abnormal cervical cytology smear was about 7 times more likely in those within the age range of 35–44 compared to pregnant women within the ages of 25 and 34 years. Women who were HIV positive were about 3 times more likely to have an abnormal cervical cytology on smear as illustrated in [Table 5].{Table 5}


The study employed LBC to screen pregnant women at their first prenatal visit to assess the pattern, prevalence and risk determinants of abnormal cervical cytology and identify those women at risk of invasive cervical cancer and offer routine cervical cancer screening as part of ANC package of AKTH.

From the studies cited from different geographical regions of Nigeria, it is evident that most of the studies carried out are on nonpregnant women, women with HIV, and other high-risk women. There are few studies generally on preinvasive cervical lesion in pregnancy in developing countries. However, the incidences of abnormal cervical cytology and HPV infection in pregnant women are generally comparable to that of nonpregnant women.[35],[36]

The prevalence of abnormal cervical cytology in this study was 13.7%. This is much higher than the prevalence of 6% reported by the works of Auwal et al.[37] in a hospital-based multi-center cross-sectional study and 11.6%[38] reported by Omole-ohonsi at the same study site. It is also higher than 10.6% from the work of Yakasai et al.[35] carried out in Kano. Despite these studies being multi-center cross-sectional studies with larger sample size, they were not among pregnant population and this could explain the observed difference in prevalence since pregnancy offers a tremendous opportunity for detection of preinvasive lesions at an earlier stage because of eversion of transformation zone in addition to the advantage of using LBC as screening which has an increased ability to detect preinvasive lesions of the cervix which our study employed. LBC has been shown to offer better clarity, uniform spread of smears, less time for screening and better handling of hemorrhagic and inflammatory smears which is in favor of smears taken during pregnancy as they are likely to be contaminated with mucus.[39],[40] It is also a higher figure compared to the 6% found in Zaria in a recent cross-sectional longitudinal study by Bakari et al.[6] although the study in Zaria was conducted among pregnant women at booking, they employed conventional pap smear as the screening tool as opposed to LBC from our study. The discrepancies between present finding and figure by Bakari et al. may be attributed but not limited to the difference in methodology. This observed difference indicates how an opportune moment the antenatal period is in detecting premalignant lesion especially when a screening tool with higher sensitivity for detection is used in the period. Incorporating cervical screening with LBC into ANC package will drastically increase coverage and detection rate.

Still within the same country, the observed prevalence of 13.7% from this present study was found to be comparable to 13.9% reported by Mosuro et al.[26] from Ibadan. Although the study was conducted among nonpregnant population, VIA was employed and the difference in sociodemographic and reproductive characteristics could explain the high figure they obtained in their study. Our finding in this study is however lower than 16.1% from Jalingo.[41] The observed difference could be due to less urban nature of Jalingo compared to Kano with the population of Jalingo having higher risk factors like the lower socio-economic class for the acquisition and persistence of HPV a necessary cause for invasive cervical cancer. Larger sample size was used and also it was a community based study unlike a hospital-based study.

The finding from this study was significantly higher than the reported prevalence of 6.8%[42] in south America, 7% in Thailand[43] and significantly higher than 0.3%[44] in south India. Even though similar study population (Pregnant women during ANC visit) and LBC was also employed, lack of an established national screening policy accounting for low screening coverage, and the differences in socio-biological characteristics making our women more liable to risk factors for HPV acquisition and persistence could explain the disparity in the prevalence between this study and the one's compared above.[42],[43],[44] The finding was comparable to the prevalence of 13.2% in Iraq,[45] although they employed conventional Pap smear, a larger sample size of 2607 was used compared to the 161 in this study, this could be the reason for the comparable prevalence.

In this study, LSIL constituted 50% of the premalignant lesion found, atypical squamous cells of undetermined significance (ASCUS) constituted 27.3% with 13.6% and 9.1% having ASC-H and HSIL, respectively. It was higher than 36.8% for LSIL but lower than 63.2% proportion for HSIL,[35] it was also significantly higher than the Ibadan[28] that reported 15.5% for LSIL, 2.8% for HSIL. The observed difference reflects the performance of LBC that was used in this study to increase detection of low-grade squamous intra-epithelial lesion (LSIL)/atypical cytology and referrals to colposcopy.[30],[40] Some women with preinvasive lesions may have been missed with conventional pap smear.

Even among developing countries like some parts of India that have incorporated cervical cancer screening as part of ANC package, the pattern is seemingly different than in our environment. In an Indian study,[46] where 300 pregnant women were screened for preinvasive lesions, only one case each for LSIL and HSIL was reported. Still in a similar study in Tamil Nadu, India, out of 200 women screened, only one was reported to have ASCUS, the remaining were inflammatory and other benign cervical cytologic changes. The difference observed with the pattern found in this study indicates that opportunistic screening is covering a substantial proportion of their women and cytopathological changes are picked at an early stage and dealt with. Many counties have now recognized the advantage of incorporating screening into routine ANC.

The risk factors for invasive cervical cancer have been well established and include early age at coitarche, multiple lifetime sexual partners, high parity, history of sexually transmitted diseases, smoking, chronic immunosuppression, history of genital warts, never or infrequent Pap testing and prolonged use of oral contraceptives.[4],[12],[15]

This study has shown a statistically significant association between increasing age, high parity, increasing number of sexual partners, and positive HIV status and the presence of preinvasive cervical cytology amongst pregnant women at their booking visit. These are factors that are interrelated and linked to HPV infection and have been well established as risk factors for cervical cancer in several literature.[4],[5],[6] However, in this study, the relationship between previous history of sexually transmitted diseases, absent of a previous Pap testing, single marital status with abnormal cervical cytology ceased to exist after adjusting for the effect of other variables in a multivariate analysis These findings were similar to those reported by Bakari et al. in zaria.[6] Reflecting the similarities in the socio-demographic and reproductive characteristics of the women in the two areas.

In this study, women within the age group 35–44 were more likely to have an abnormality in their cervical smear similar to the findings of Yakasai et al.,[35] reflecting the natural history of HPV infection. Pregnant women at booking whose ages fall between 35 and 44 years are >6 times more likely to have an abnormal cervical cytology compared to pregnant women in the younger age group.

This study has demonstrated that there is a statistically significant Association between increasing number of sexual partners and previous history of STI with abnormal cervical cytology. Even before data convincingly linked HPV to the development of cervical cancer, it was well recognized that various aspect of a patient's sexual history put women at increased risk for developing preinvasive and subsequent invasive lesions of the cervix.[15] Overall, the number of recent and total lifetime male partners increases the rate of high-risk HPV infection. In addition, co-infection with other STI has been associated with increased susceptibility to HPV infection. Both bacterial vaginosis and trichomoniasis are strongly associated with HPV infection.[47]

This study has shown that pregnant women who are HIV positive were more likely to have preinvasive cervical lesions in this study. HIV infection is strongly associated with HPV infection.[15],[39] Several studies have shown that higher prevalence and persistence of HPV are all more frequent in HIV positive women. Primarily, a functional immune system is required to keep HPV in a latent and subclinical state. Thus, HIV infection, in addition to other forms of immunosuppression, predisposes to progression and reactivation of HPV infection, as well as promotion of viral oncogenesis in HIV-associated CIN.[39] This study has clearly demonstrated that pregnant women who are HIV positive are almost 3 times more likely to have an abnormal cervical cytology in their smears compared to pregnant women who are HIV negative.

Several international meta-analyses have published that, women defined as belonging to a low socioeconomic class were found to have twice the risk of invasive cervical cancer compared to those in a high socio-economic class.[48] However, this study did not establish an association between social class and the presence of preinvasive cervical lesion. This is contrary to the findings in Kano[40] by Auwal et al. and also those from Salih et al.[49] In this study only one patient belonged to the low socio-economic class. The reason for this being that this study was carried out at AKTH, a tertiary hospital located at the heart of Kano, where health services are paid for, hence majority of the patronizers are of middle to high social class as opposed to most of the general hospitals in Kano where the other studies were conducted where free health services are offered including ANC. Ultimately, those of low socioeconomic class would rather patronize the general hospitals.

This study shows an association between increasing parity with the presence of an abnormal cervical cytology similar to findings of some studies,[35],[41] but is contrary to the findings of Bakari et al.[6] and Seda et al.[42] Although literature has reported a dose-dependent increase in risk with numbers of live births. Although this epidemiologic association is firmly established, the explanatory mechanism is not quite clear. This may explain the difference in findings from different studies. Some of the possible mechanisms underlying the association between it and cervical neoplasia include trauma during parturition, hormonal changes with pregnancy, immunosuppression and altered anatomy of the transformation zone, specifically eversion.[15]

This study did not demonstrate an association between marital setting and the presence of abnormal cervical cytology. Contrary to the belief that some socio-cultural practices such as early marriage, high parity and to certain extent polygamy identified as factors that increased the vulnerability of women to cervical cancer. Most polygamy in this environment is a closed marital setting and those not equate to multiple sexual partners. Lack of association reflects the marriage fidelity in this environment.

Several studies, as well as collaborative pooled analysis and registry linkages, among group of women infected with carcinogenic HPV have shown that smokers are at increased risk compared with nonsmokers.[50] Most studies confirmed that the current smoking increases the prevalence, persistence of high risk type as well as delayed clearance of HPV infection compared with nonsmokers and former smokers.[50] Cigarette smoking was not found among any of the women in this study similar to the finding of Omole-ohonsi at same study site.[38] This is not surprising however since smoking is considered to be socially unacceptable among women in the majority of African communities particularly in our predominantly Islamic community.[38]

Although the use of oral hormonal contraceptives could plausibly potentiate the carcinogenicity of HPV infection, because transcriptional regulatory regions of HPV-DNA contain hormone-recognition elements and transformation of cells in vitro with viral DNA is enhanced by hormones, several studies found an elevated risk of ICC among HPV-positive women who used oral contraceptives for >5 years. This study this did not attempt at establishing an association between them because no single respondent gave a positive history of oral hormonal usage continuously for >5 years.


This study has shown a significantly high prevalence of premalignant lesions of the cervix among antenatal clients with a value of 13.7%. LSIL was the most common pattern accounting for 50% of the abnormal cervical cytology. It has identified pregnant women at increased risk of preinvasive cervical lesions namely; those within ages 35–44 at booking, who are HIV positive, with high parity (>5), and those with increasing number of sexual partners since coitarche. Therefore, integration of cervical cytology screening into our routine ANC package will serve as a tremendous opportunity for detection of preinvasive lesions at an early stage because of eversion of the transformation zone.

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Conflicts of interest

There are no conflicts of interest.


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