|Year : 2017 | Volume
| Issue : 4 | Page : 160-167
Incidence and risk factors of cervical dysplasia among human immune deficiency virus positive and human immune deficiency virus negative women at Aminu Kano Teaching Hospital
Zakari Muhammad1, Iman Haruna Usman1, Zainab Ahmed Datti1, Attah Rapheal Avidime1, Shuaibu Adavuruku Danjuma1, Atanda Akinfenwa Taoheed2, Aisha Abdullahi Suleiman3
1 Department of Obstetrics and Gynaecology, Aminu Kano Teaching Hospital, Bayero University, Kano, Nigeria
2 Department of Histopathology, Aminu Kano Teaching Hospital, Bayero University, Kano, Nigeria
3 Department of Nursing Science, Aminu Kano Teaching Hospital, Bayero University, Kano, Nigeria
|Date of Web Publication||17-Apr-2018|
Dr. Zakari Muhammad
Department of Obstetrics and Gynaecology, Aminu Kano Teaching Hospital, Bayero University, Kano
Background: HIV infection is a risk factor for cervical cancer and both diseases are prevalent in Nigeria. HIV positive women are at greater risk of cervical dysplasia than HIV negative women which may be as a result of immunosupression, hence adding more burdens to their already worsening health condition. It has become relevant to screen these women early and refer for appropriate and effective therapeutic intervention. Objective: To compare the incidence and risk factors of cervical dysplasia among HIV positive and HIV negative women at Aminu Kano Teaching Hospital, Kano. Methods: This was a comparative cross sectional studyl, which involved HIV positive women attending HIV clinic and HIV negative women attending the gynecological clinic at Aminu Kano Teaching Hospital. A cohort of 150 consenting HIV- positive women not on HAART and 150 HIV- negative women, selected by systematic random sampling were sent for Pap smear examination. On the same day blood samples were taken from antecubital vein and sent for both CD4 count and viral load among the HIV positive group. A pretested questionnaire was administered to the women of both groups on same day to determine the presence or absence of risk factors of cervical dysplasia in them. The results obtained were recorded using proforma and analyses of risk factors of cervical dysplasia was done using Chi square test and Fisher exact test to compare variables between those with normal and abnormal smears and student t test to determine the relationship of lesions with CD4count and viral load among the HIV positive women. Results: The incidence of cervical dysplasia among HIV- positive women was 49 (32.7%) and was significantly higher than 12(8%) found among the HIV- negative. Age ≥ 35years and parity ≥5, early coitarche, multiple sexual partners, low-socioeconomic status, cigarette smoking did confer some risk of dysplasia however. This study also showed that among the HIV positive group, CD4 count was inversely associated with risk of cervical dysplasia and women with a CD4 count <500 cells/mm3 were at greater risk of cervical dysplasia compared with women with CD4counts>500 cells/mm3. Conclusion: It Ais important to carryout cervical smear screening for HIV-positive women, especially those with a CD4 count<500 at first contact.
Keywords: Aminu Kano Teaching Hospital-Kano, cervical dysplasia, human immune deficiency virus-positive women, incidence, risk factors
|How to cite this article:|
Muhammad Z, Usman IH, Datti ZA, Avidime AR, Danjuma SA, Taoheed AA, Suleiman AA. Incidence and risk factors of cervical dysplasia among human immune deficiency virus positive and human immune deficiency virus negative women at Aminu Kano Teaching Hospital. Sahel Med J 2017;20:160-7
|How to cite this URL:|
Muhammad Z, Usman IH, Datti ZA, Avidime AR, Danjuma SA, Taoheed AA, Suleiman AA. Incidence and risk factors of cervical dysplasia among human immune deficiency virus positive and human immune deficiency virus negative women at Aminu Kano Teaching Hospital. Sahel Med J [serial online] 2017 [cited 2018 May 23];20:160-7. Available from: http://www.smjonline.org/text.asp?2017/20/4/160/230259
| Introduction|| |
Cervical cancer remains a major health issue among women in developing countries, especially in developing countries. Worldwide, it is the second most common malignancy in women ,, and the most common cause of cancer-related morbidity and mortality in women in low resource countries. There are estimated over 500,000 new cases and 250,000 deaths each year globally, of which 80% occur in developing countries.,,,, Cervical cancer is the most common malignancy of the female genital tract in Nigeria, accounting for 70.5% of gynecological malignancies in Maiduguri, 59.2% in Kano, 60% in Ilorin, 74% in Jos, 74.6% in Benin, and 77% in Zaria.,,,,, Data from Ghana and Kenya have shown that cervical cancer accounted for 57.8%, 70%–80% of gynecological cancers, respectively., This high prevalence is due to high incidence of sexually transmitted diseases in Sub-Saharan Africa and the fact that this correlates with human papillomavirus (HPV) infection forming the core of cervical cancer.
In the United States of America, cervical cancer now ranks 14th in frequency, accounting for 1.5% of all new cases of cancer and 1.3% of cancer-related deaths in women. In Sweden, it constitutes 2.6% of female malignant cancers. Currently, an estimated 33.3 million individuals worldwide are living with Human Immune Deficiency Virus (HIV/AIDS), approximately 68% of whom live in Sub-Saharan Africa. Globally, over 50% of all those living with HIV are females. Nigeria ranks third in the list of all countries for the total number of people living with HIV, with 1.7–4.2 million people infected with the virus. Etiological factors for both cancers of the cervix and HIV/AIDS are sexually transmitted and found most prevalent among the low socioeconomic, promiscuous smoking women with HPV infection. Cancer of the cervix is classified as AIDS-defining cancer by the US Centers for Disease Control and Prevention, and it runs a more fulminant course in women infected with HIV. The natural history of cervical cancer is well known as it progresses from a well-defined premalignant state called cervical intraepithelial neoplasia (CIN). It takes an average of 10-20 years for CIN to progress to invasive cervical cancer and may progress from low-grade intraepithelial lesion (LSIL) to high-grade intraepithelial lesion (HSIL). HSIL may then progress to invasive cancer. The risk of progression from LSIL to HSIL to invasive cancer is low, with a small minority of about 11% of untreated LSIL women eventually progressing to HSIL and invasive cancer over several decades. This long premalignant phase allows for preventive interventions.
Compared to immunocompetent women, HIV-positive women have a higher prevalence, incidence, and progression rate of precancerous cervical lesions. HIV-positive people are more likely to be infected with HPV infection than HIV-negative people. The incidence of cervical dysplasia is 4–5 times higher among HIV-infected than HIV-negative women and girls.,, A clear causal relationship has been established between HPV infection and the development of cervical cancer. Cervical cancer and HIV infection are major public health problems in Nigeria and other parts of Sub-Saharan Africa,, further emphasizing the importance of routine screening in this subset of women.
| Methodology|| |
Background of study area
The study area was Aminu Kano Teaching Hospital, which is a tertiary health institution in Kano state, situated in the North-Western geopolitical zone of Nigeria, under the Federal Ministry of Health and was commissioned on August 24, 1988. It is a 500-bed hospital located in Kano; the largest commercial center of northern Nigeria, this hospital receives clients from within Kano and the neighboring states of Jigawa, Katsina, Kaduna, Bauchi, and Zamfara states. Majority of the patients are indigenous Hausa and Fulani, although the Igbo and Yoruba ethnic groups also constitute a substantial proportion of the clients. Most of the people are traders, farmers, businessmen, and civil servants and majority are Muslims.
The study was a comparative cross-sectional analytical study of the risk factors of cervical dysplasia among HIV-positive women attending HIV clinic and HIV negative attending gynecology clinic at Aminu Kano Teaching Hospital, from October 1, 2016, to December 31, 2016.
The sample size was determined using the statistical formula for a comparison of proportions as follows:
n = minimum sample size
Zα = Standard Normal deviate set at 95% confidence
Level = 1.96
Zβ= Power of the test to detect difference set at
95% confidence level = 1.64
P1 = Prevalence of cervical dysplasia among HIV negative women (obtained from a previous study).23
P2 = Prevalence of cervical dysplasia among HIV-positive women (obtained from a previous study).
q1 = Complementary probability (1 − p1) = (1 − 0.116) = 0.88
q2 = Complementary probability (1 − p2) = (1 − 0.297) = 0.703
n = 129.84
n = 130 respondents in each group + 10% attrition = 130 + 13 = 143
Hence, this would account to approximately 150 respondents in each group
The above sample size was retrieved over a period of 3 months.
The recruitment was by a systematic random sampling method among consented HIV-positive and HIV-negative women of reproductive age until a sample size of 150 respondents was obtained in each group. For the HIV positive, the sample population of 1049 was divided by sample size of 300 giving a sampling interval of four. The total number of gynecological patients seen per month (1000) was divided by sample size of 300 giving a sampling interval of 3.
Questionnaires were manually checked for completeness, missing, and wrong entries. Data were analyzed Using the Statistical Package for the Social Sciences (SPSS) version 17.0. Data presentations were in tabular and graphical forms as appropriate. Chi-square test and Fisher's exact test were used to determine the statistical relationship between proportions of respondents and scores for different variables. Quantitative values (CD4 count and Viral load) were compared for statistical significance using Student's t-test. The level of statistical significance was set at <0.05.
Instruments and method of data collection
The women were counseled to secure their consent to participate in the study with respect to responding to the questionnaire and collection of blood sample. All consented women were recruited for the study
Semi-structured questionnaire was administered for the study. There were two questionnaires, one for the HIV positive and another for the HIV-negative respondents. They were both interviewer-administered questionnaires. The researcher and two other attending doctors administered the questionnaire after an orientation on how to administer was given.
The questionnaires contained questions on sociodemographic data, sexual history, gynecological history, medical history, history of prior STI, and history of HAART use at the time of the study. Clients with abnormal vaginal discharge, ulcers, warts, and any abnormal cervical findings were labeled as having sexually transmitted infection. Clients were classified into high and low socioeconomic status using Olusanya social class. Clients with social class 1, 2, and 3 were graded as low and those with social class 4 and 5 as high. Clients for the control group were recruited after conducting an advocacy visit to 4 local governments (Tarauni, Kano municipal Kumbotso, and Nasarawa). These clients were told the services to be offered were free. They were told to come to the gynecology clinic which holds every day by 2 pm. All recruited clients had HIV screening test. Those positive were sent to PEPFAR and those negative sent to gynecology clinic. Questionnaires were coded with affixed serial numbers of the clients thus blinding the cytopathologist to the identity of study participants.
All patients had their HIV status confirmed by Western blot following the presentation of a positive screening test. Blood sample (4 ml) was collected from all participating clients from the antecubital vein, using a 5 ml plastic disposable syringe. This was done by the researcher, two other resident doctors and a laboratory scientist on the same day with the collection of cervical smears. Each sample for a particular client was coded for easy identification. Each sample was transferred to a clean test tube and allowed to clot. HIV-RNA viral load was determined by nucleic acid amplification and results were expressed as the number of RNA copies/ml. Values of 400copies/ml or fewer were regarded as undetectable. CD4 count was measured using flow cytometry and was reported as copies per cubic millimeter of blood (copies/mm 3). These services offered (CD4 count and viral load) were free.
The patients were subjected to both speculum and pelvic examinations to detect any gross abnormal lesions that would be excluded from the study and also detect any abnormal vaginal discharge. These examinations were performed by both the researcher and three other residents and a midwife (working in HIV and gynecology clinics trained to perform both speculum and pelvic examinations).
General and abdominal examinations were performed by the researcher and three other residents followed by collection of Papanicolaou (pap) smear using a wooden spatula. The Pap smear More Detailss were collected during the proliferative phase of the women's menstrual cycle. The women were told to avoid coitus, douching or vaginal insertion that could interfere with the readings before the test. Collection of the Pap smears was carried out with women in dorsal position and inserting a sterile speculum lubricated with water. The cervix was exposed using Cusco speculum and Ayre's spatula inserted and rotated through 360°C. All smears were placed on 2 prelabeled slides for convenience and immediately fixed using 95% alcohol and samples sent to histopathology laboratory for testing.
The slides were stained according to the Pap staining technique. The fixed slides were stained first in Harris hematoxylin, then decolorized with acid alcohol and rinsed in Scott's tap water. They were then stained in orange G stock solution and finally stained with Eosin Azure 50. The slides were further rinsed in 95% alcohol, cleared in xylene, and mounted in a neutral synthetic resin medium. The researcher and cytotechnologist prepared the slides and Cytopathologist examined the Pap smears and reported using Bethesda 2001 system terminology. Blood samples for CD4 count and viral load assays were taken on same day as the Pap smears. Women with abnormal smears were referred for further evaluation in the gynecology clinic of the hospital. The results in each group were divided into women that had normal and abnormal smears and risk factors among each group determined. The ensuing data were subjected to statistical analyses using Chi-square and Fisher's exact test and presented in tabular form.
The study variables of interest were age and parity of the women, age at coitache, marriage and first childbirth, marital status, number of sexual partners, educational and socioeconomic status, history of vaginal discharge or vaginal bleeding, contraceptive use, smoking, and genital ulcers.
Approval for the study was obtained from the hospital's ethical committee.
| Results|| |
A total of 300 samples were collected out of which 150 were HIV positive and 150 were HIV negative. The mean age of respondents was 29.81 ± 7.2 years for the HIV-positive group and 31.9 ± 9.8 years for the HIV-negative group. Ages of the two groups ranged from 15 to 49 years.
[Table 1] shows the sociodemographic features of respondents. There was no significant difference among the ages of the respondents. HIV-positive women had more formal education than HIV negative (50% vs. 42.4%) although it was not statistically significant (P = 0.164). A greater number of the HIV negatives (87.4%) were married while the HIV positives are either single (8.7%), widowed (33.3%), or divorced (18.0%). Almost all the respondents both HIV positives (98.0%) and HIV negatives (98.7%) were of low socioeconomic status, but this was not statistically significant (P = 0.652).
|Table 1: Demographic and socio-economic characteristics of the study population|
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[Table 2] shows that the incidence of positive smears in HIV-positive women was almost 25% higher than in HIV-negative respondents and this was found to be statistically significant (P = 0.000). Thus the study showed the incidence of cervical dysplasia to be (32.7%) among the seropositive and (8.0%) among the seronegatives.
[Table 3] shows the pattern of risk factors among HIV positive and negative groups. The percentage of smokers was greater among seropositive than seronegatives (18.7% vs. 1.3% P = 0.000). HIV-positive women had earlier coitache at ages less than 15 when compared with their negative counterparts (43.3% vs. 7.3% P = 0.000) HIV-positive clients also had greater number of sexual partners (24.7% vs. 0.0% P = 0.000). The number of the respondents who had ever had sexually transmitted infection was greater among seropositive clients (61.4% vs. 22.7% P = 0.000). The HIV-positive group also had a greater number of cigarette smokers than HIV negative group (18.7% vs. 1.3% P = 0.000). Oral contraceptive use was greater among the HIV negatives (22.0% vs. 11.3% P = 0.213). Almost all the respondents were of low socioeconomic status (98.0%vs. 98.7% P = 0.000). Higher parity was seen more significantly among the HIV positives than negative (41.3% vs. 21.2% P = 0.000).
[Table 4] shows multivariate analyses of characteristics associated with cervical dysplasia. Smoking appeared to increase the risk of cervical dysplasia by about 4 times greater than those that did not smoke and 1.4 times higher risk if they were secondary smokers. Sexually transmitted infection increases the risk of cervical dysplasia by about 5 times. While early coitarche increased the risk, those with coitarche between the ages 15–30 years are 0.1 times less likely going to develop cervical dysplasia and those >30 are 0.8 times less likely of to develop cervical dysplasia. Those with parity >5 are almost 4 times more likely going to develop cervical dysplasia when compared to those with low parity.
|Table 4: Multivariate analyses of characteristics associated with cervical dysplasia|
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[Table 5] shows an independent t-test which shows that the difference between the mean CD4 count of respondents with normal and abnormal cervical cytology is statistically significant. T =16.6, P = 0.000, 95% confidence interval (CI) (761.8, 967.1), df = 127.7. It also shows that the difference between the mean viral load of respondents with normal and abnormal cervical cytology is statistically significant, t = -3.6, P = 0.001, 95% CI [-38580.3,-10723.3], df = 48.
|Table 5: Independent t-test and descriptives statistics for cd4 count and viral load by cervical cytology|
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| Discussion|| |
In this study, HIV-positive women had higher incidence of cervical dysplasia than HIV-negative women (32.7% vs. 8%). The high incidence of 32.7% among HIV-positive women is similar to studies conducted in Port Harcourt (34.4%), Maiduguri (31.3%) but slightly higher than the 29%, and 21% from Jos, 10.9% from Lagos, 28.7% from Zaria. This may be due to differences in sample size, and population characteristics. The incidence among the HIV negatives of 8% in this study is comparable to studies by Jos (6%), Maiduguri (7.8%), and slightly lower than earlier studies in Kano 11.6%, 10.63%, and 23.8% in Ilorin and higher than the 4.3% from Lagos. A comparative study between Baltimore, United States, and Thailand , reported an incidence of 13% and 10.5%, respectively, among seropositives with the highest reported incidence in Zambia 76%. The high incidence seen in developing countries when compared to developed countries may be attributed to the high incidence of sexually transmitted infection in developing countries 
Advancing maternal age, early coitarche, increasing parity, sexually transmitted infections, increasing number of sexual partners, multiparty, and smoking were found to be significant risk factors in this study among both groups and agrees with various studies., Early marriage which depicts early coitarche is a common practice in Northern Nigeria, and this highly increases the girls vulnerability to cancer of cervix due to the dynamic nature of transformation zone at an early age making it more prone to infections., Early coitarche increases risk of HPV infection. The mechanism by which early coitarche is linked to cervical carcinogenesis is related to steroid hormonal influence on HPV infection and host immune response to HPV during preadolescence and adolescence. Early coitarche was a risk factor found statistically significant in this study and agrees with a study in Zaria. Although the use of oral contraceptive increases the risk of cervical cancer, this was not demonstrated in this study but was seen to be statistically significant in a study by Omole. Smoking was found to be a risk factor for the development of cervical dysplasia in this study and was more frequently seen among the seropositives in this study. This may be due to a more adventurous nature of the group or other reasons not identifiable by this study. Smoking as identifiable by Omole  increases the risk of cervical dysplasia by 3–4 times and is similar to what was obtained in multivariate analyses in this study. It is obvious that low socioeconomic status puts a strain on moral values and increases sexual promiscuity and this increases the risk of sexually transmitted infection especially HPV, hence, the development of cervical dysplasia. Low socioeconomic status was found to be statistically significant for the development of cervical dysplasia among both groups in this study. These risk factors were found to be characteristics more associated with HIV positive than negative. Impairment of immunity as an expression of a low CD4 lymphocyte count appears to play an important role in cervical neoplasia. Gemignani et al. studied the relation between CD4 lymphocyte counts and the stage of cervical neoplasia in a population of HIV-negative women. They found that women with invasive squamous cell carcinoma had significantly lower CD4counts compared with patients with CIN. This study showed that the CD4 count was inversely correlated with risk of cervical dysplasia, and women with a CD4 count <500 cells/mm  were at greater risk of cervical dysplasia compared with women with CD4 counts >500 cells/mm. This finding is in accordance with several other studies involving HIV-positive women,, Davis et al. reported that the strongest predictor of genital dysplasia was a nadir CD4 and CD4 count <200 cells/mm. Prolonged CD4 lymphopenia in patients infected with HIV results in defective T-cell proliferation regardless of the current CD4 count or viral load. In this study, the median viral load was significantly higher in patients with cervical dysplasia than in those without it. Furthermore, viral load >10,000 copies/mL was associated with SIL in multivariate analysis. However, a high level of viral copies does not always predict the risk of cervical dysplasia, because some studies have failed to show a positive association. For instance, Agaba et al. observed that although the viral load was higher in patients with SIL, it was not predictive of SIL.
High incidence of cervical dysplasia was noted among HIV-infected women in Aminu Kano Teaching Hospital. Even though the risk factors for cervical dysplasia in this study are similar among both groups though greater proportion was seen among sero positive. Among the seropositive, decreased CD4 cell counts, and increasing viral load were associated with cervical dysplasia. CD4 cell counts <500 cells/mm  and HIV RNA viral loads >10,000 copies/mL were significantly associated with higher grade lesions.
| Conclusion|| |
It can be concluded from this study that not only is there need to carry out cervical smear screening for all women, the need is, even more, pressing for the HIV positive, especially those with a CD4 count <500 at first contact.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]