International Journal of Gynecology and Obstetrics 125 (2014) 103–106

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CLINICAL ARTICLE

Abnormal cervical cytology among HIV-positive women in Nigeria Goddy Bassey a, Israel Jeremiah b,⁎, John I. Ikimalo c, Preye O. Fiebai a, Boma P. Athanasius c a b c

Department of Obstetrics and Gynecology, University of Port Harcourt Teaching Hospital, Port Harcourt, Nigeria Department of Obstetrics and Gynecology, Niger Delta University, Wilberforce Island, Nigeria Department of Anatomical Pathology, University of Port Harcourt Teaching Hospital, Port Harcourt, Nigeria

a r t i c l e

i n f o

Article history: Received 20 June 2013 Received in revised form 29 October 2013 Accepted 27 January 2014 Keywords: CD4 count Cervical cytology HIV-positive women

a b s t r a c t Objective: To determine the prevalence of abnormal cervical smears and high-grade lesions among HIV-positive and HIV-negative women, and to assess the relationship between severity of disease and CD4 count. Methods: In a prospective cross-sectional comparative study, 250 HIV-positive and 250 HIV-negative women attending the University of Port Harcourt Teaching Hospital, Port Harcourt, Nigeria, were enrolled between January and March 2012. Cervical smear samples were collected from participants, examined, and reported via the Bethesda system. Data management and analysis was done with SPSS. Differences between the 2 study groups were determined by χ2 test and Student t test. Results: The prevalence of abnormal cervical smears was significantly higher among HIV-positive women (34.4%) than among HIV-negative women (20.2%) (P b 0.01). The proportion of high-grade lesions was significantly higher among HIV-positive women (23.5%) than among HIV-negative women (8.2%) (P = 0.025). HIV-positive women with a CD4 count below 500 cells/mm3 had significantly more abnormal cervical smears (28.3%) compared with those with a CD4 count of 500 cells/mm3 or more (6.1%) (P = 0.04). Conclusion: HIV-positive women were found to be at significantly greater risk of developing abnormal cervical cytology and high-grade lesions compared with HIV-negative women. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction Cervical cancer is the most common genital tract malignancy in Nigeria [1]. It accounts for 12% of all cancers in women, and 60%–80% of cases are first seen in advanced clinical stage with poor prognosis in low-resource countries [2,3]. Fortunately, the condition has a recognized premalignant stage, which takes up to 10 years to develop into malignancy [4,5]. Detection of the disease in this premalignant stage has been recognized as a reliable way of reducing the morbidity and mortality from cervical cancer [5,6]. However, such results are seen with population-based screening and not with the opportunistic screening that is carried out in low-resource countries such as Nigeria [2,7]. The Papanicolaou (Pap) smear has been the traditional method of screening for premalignant lesions of the cervix [5]. The modified Bethesda system of classifying cervical cytology is currently the preferred method of interpreting Pap smear. The system was first initiated in 1988 but was modified in 2001 to reflect current understanding of the disease process and to eliminate the ambiguity associated with the interpretation and management of atypical cells of undetermined significance [8–10]. In the modified Bethesda system, Pap smears are classified as negative for intraepithelial lesions or cancer, or as lowgrade squamous intraepithelial lesion (LGSIL), atypical squamous cells of undetermined significance (ASC-US), atypical squamous cells cannot ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Niger Delta University, Wilberforce Island, Bayelsa State, Nigeria. Tel.: +234 8035009848. E-mail address: [email protected] (I. Jeremiah).

exclude high-grade lesion (ASC-H), atypical glandular cells of undetermined significance (AGC-US), atypical glandular cells favors neoplastic (AGC-H), high-grade squamous intraepithelial lesion (HGSIL), or invasive cancer [9,10]. Human papilloma virus (HPV) has been established as the etiologic agent for cervical dysplasia and cervical cancer and, among the numerous serotypes, HPV16 and HPV18 are regarded as the most virulent [1,11,12]. Most cases of HPV infection are usually cleared by the host immune system. However, immunocompromised individuals, such as HIV-positive women, are at increased risk of having persistent HPV infections [13]. The first case of HIV was documented in 1981. Since then, the disease has become a pandemic: in 2007, there were an estimated 2.1 million deaths, and 33.2 million people were living with the disease [14]. Most cases of HIV occur in Africa, and Nigeria is second only to South Africa in terms of HIV prevalence [14]. Owing to repeated findings of cervical cancer among HIV-positive women, moderate and severe cervical dysplasia have been designated as early symptomatic HIV infection, and invasive cervical cancer has been designated as an AIDS-defining condition by the Centre for Disease Control [15]. HIV-infected women are at greater risk of developing and harboring severe cervical dysplasia. With the use of highly active antiretroviral therapy (HAART), which has improved the life expectancy of HIV-infected women, there is a need to produce management guidelines for the screening and treatment of cervical dysplasia among these women [16]. Judging from the above, it is obvious that HIV-infected women may require greater

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surveillance in order to detect premalignant lesions of the cervix before they progress to cancer. Unfortunately, premalignant lesions do not have characteristic symptoms or signs, and screening remains the only method of detecting them. The aim of the present study was to determine the prevalence of abnormal cervical smears and high-grade lesions among HIV-positive and HIV-negative women, and to assess the relationship between severity of disease and CD4 count, with the anticipation that findings from the study might facilitate the adoption of a policy of routine screening for cervical cancer among HIV-positive women in Nigeria. 2. Materials and methods In a prospective cross-sectional comparative study, 250 HIV-positive and 250 HIV-negative women attending the HIV clinic and the general outpatient clinic of the University of Port Harcourt Teaching Hospital, Port Harcourt, Nigeria, were enrolled between January 1 and March 31, 2012. Approval for the study was obtained from the ethical committee of the University of Port Harcourt Teaching Hospital, and all women provided consent for participation. The sample size was calculated from the formula n = Z2 × P × (1–P)/d2 [17], where n is the sample size; z is the proportion of normal distribution corresponding to the required significance level of 5% (1.96); P is the proportion of HIV-positive women with abnormal cervical cytology observed in a similar study (20%) [18]; and d is the relative precision or tolerable error of the estimate from the study (5%). Thus, n = (1.96)2 × 0.2 × (1–0.2)/(0.05)2 = 246. Therefore, the minimum sample size was 246 women in each group. Women who gave consent, and were neither menstruating nor had vaginal discharge were eligible for the study. Women who had had sexual intercourse or vaginal douching 48 h before the test, those who were not yet sexually exposed, and those who had had a Pap smear in the past 6 months were excluded from the study. Women who had obvious lesions on the cervix were also excluded, but were referred to the gynecology clinic for further evaluation. The researchers gave a health talk at the beginning of the clinic on cervical cancer and also discussed the purpose and conduct of the study. All women were encouraged to have the screening whether or not they took part in the study. For the study, a simple random sampling technique was used to select 250 HIV-positive women from the HIV clinic and 250 HIV-negative women from the general outpatient clinic. Ten women were selected daily from either clinic, and the required sample size was achieved over a 3-month period. Women in the general outpatient clinic who met the eligibility criteria received voluntary counseling and testing for HIV by a trained HIV counselor; those who were HIV-negative were selected for the study, and those who were HIV-positive were referred to the HIV clinic for further care. The HIV test was performed using a rapid kit test (Alere Determine HIV-1/2; Alere Medical, Matsudo-shi, Japan). A designed protocol was used to obtain sociodemographic information from the participants. Other relevant information was obtained from the case files of the participants. Participants were grouped into socioeconomic class via a standard classification system devised by the Office of Population Census and Surveys in London in 1991 [19]. Cervical smears were collected by trained personnel. A senior cytotechnician assisted in the staining of the smears, and the smears were read by a consultant histopathologist and reported via the modified Bethesda system. The slides were coded and the histopathologist was blind to whether the slides were from the HIV-positive or HIVnegative groups. Repeat checks on all slides were carried out before the final reports were written. The Department of Anatomical Pathology at the University of Port Harcourt Teaching Hospital is engaged in both internal and external quality assurance programs that ensure the validity of its reports. Participants who had high-grade lesions were referred for colposcopy, whereas those with other forms of abnormal cytology were counseled for a repeat Pap test in 6 months.

All data obtained were entered into a spreadsheet using SPSS version 16 (IBM, Armonk, NY, USA), which was also used for analysis. The mean, standard deviation, and percentages of variables were calculated. Significant differences in categorical variables between the 2 study groups were determined by χ2 test. Differences were considered significant at a P value of less than 0.05. 3. Results During the study period, 247 Pap smears collected from 250 HIVpositive women were satisfactory, among which 85 (34.4%) showed abnormal cervical cytology and 162 (65.6%) had normal cytology. Among 248 satisfactory smears in the HIV-negative group, 49 (19.8%) showed abnormal cervical cytology. This difference in abnormal cervical cytology between the HIV-positive and HIV-negative groups was significant (P b 0.01). Table 1 shows the proportion of the various grades of abnormal cervical cytology among the HIV-positive and HIV-negative groups. The mean age of participants in the HIV-positive group was 33.3 ± 7.9 years (range 17–56 years), whereas that in the HIV-negative group was 37.6 ± 10.2 years (range 19–60 years). Table 2 shows the relationship between age and abnormal cervical cytology in both groups. HIV-positive women who were less than 40 years of age were significantly more at risk of having abnormal cervical cytology than were HIV-negative women of a similar age (P b 0.01), and HIV-positive women aged 40 years or older were significantly more likely to harbor high-grade lesions compared with their HIV-negative counterparts (P b 0.01). The mean parity in HIV-positive and HIV-negative groups was 1.6 ± 2.1 and 2.6 ± 2.3, respectively. The sociodemographic characteristics of the participants and risk factors for cervical dysplasia are shown in Table 3. All the women who had previously had a Pap smear in both groups and 80.0% (n = 107) of those who had knowledge of Pap smear had a tertiary level of education. None of the participants admitted to cigarette smoking. In the HIVpositive group, 2 women (0.8%) had previously been treated for vulva warts, and 2 women were found to have them during vaginal examination. None of the women in the HIV-negative group had vulva warts. Among the HIV-positive women, 236 (94.4%) had been on HAART for at least 1 year. The mean CD4 lymphocyte count was 380 ± 262.0 cells/mm3. Seventy (38.0%) of 184 women with a CD4 count of less than 500 cells/mm3 had abnormal cervical cytology, whereas 15 (23.8%) of 63 women with a CD4 count of 500 cells/mm3 or higher had abnormal cytology (P = 0.04). Five (33.3%) of the 15 women with an abnormal Pap smear and a CD4 count of 500 cells/mm3 or higher were classified as HGSIL, whereas 15 (21.4%) of the 70 women with an abnormal smear and a CD4 count of less than 500 cells/mm3 were classified as HGSIL (χ2 = 0.96, P = 0.33). Tables 4 and 5 show the relationship between CD4 count and abnormal cervical cytology. 4. Discussion The prevalence of abnormal cervical cytology among HIV-positive women of 34.4% detected in the present study is higher than that of

Table 1 Distribution of abnormal Pap smears in the 2 study groups.a Group

HIV-positive HIV-negative P value

Type of abnormal Pap smear

Total

LGSIL

ASC-US

HGSIL

AGC-US

38 (44.7) 16 (32.7) 0.17

24 (28.2) 27 (55.1) 0.002

20 (23.5) 4 (8.2) 0.025

3 (3.5) 2 (4.1) 0.07

85 (100) 49 (100)

Abbreviations: AGC-US, atypical glandular cells of undetermined significance; ASC-US, atypical squamous cells of undetermined significance; HGSIL, high-grade squamous intraepithelial lesions; LGSIL, low-grade squamous intraepithelial lesions. a Values are given as number (percentage).

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Table 2 Distribution of abnormal cervical cytology in the 2 study groups by age range.a Age range, y

b20 20–29 30–39 40–49 ≥50 Total

Overall incidence

LGSIL

ASC-US

HGSIL

AGC-US

HIV+

HIV–

HIV+

HIV–

HIV+

HIV–

HIV+

HIV–

HIV+

HIV–

1 (0.4) 97 (38.8) 104 (41.6) 25 (10.0) 12 (4.8) 250 (100)

4 (1.6) 52 (20.8) 78 (31.2) 84 (33.6) 32 (12.8) 250 (100)

– 15 (15.5) 18 (17.3) 4 (16.0) 1 (8.3) 38

– 2 (3.8) 5 (6.4) 7 (8.3) 2 (6.3) 16

– 9 (9.3) 11 (10.5) 3 (12.0) 1 (8.3) 24

– 1 (1.9) 2 (2.6) 14 (16.6) 10 (31.3) 27

– 2 (2.1) 1 (0.9) 7 (28.0) 10 (83.3) 20

– – 1 (1.3) 1 (1.2) 2 (6.3) 4

– – 2 (1.9) 1 (4.0) – 3

– – – 1 (1.2) 1 (3.1) 2

Abbreviations: AGC-US, atypical glandular cells of undetermined significance; ASC-US, atypical squamous cells of undetermined significance; HGSIL, high-grade squamous intraepithelial lesions; LGSIL, low-grade squamous intraepithelial lesions. a Values are given as number (percentage).

10.9% reported by Anorlu et al. [20] in Lagos and 31.3% reported by Chama et al. [21] in Maiduguri, Nigeria. However, the present rate is lower than that of 38.3% and 68.0% reported by Massad et al. [22] in the United States and Agaba et al. [17] in Jos, Nigeria, respectively. Apart from the larger sample sizes in the studies of Massad et al. [22] and Agaba et al. [17], the prevalence of HPV infection and the degree of immunosuppression might account for the differences observed, especially considering that more than 90% of the present study participants had been on HAART for at least 1 year. The significant difference in the prevalence of abnormal cervical cytology between the 2 groups in the present study is consistent with other studies, and supports the fact that, compared with HIV-negative women, HIV-positive women are at greater risk of developing abnormal cervical cytology and are significantly more likely to have abnormal smears due to HGSIL [20,22]. The findings that HIV-positive women who were younger than 40 years were significantly at risk of developing abnormal cytology (low-grade lesions) and that those older than 40 years were significantly more likely to have high-grade lesions

Table 3 Sociodemographic and risk factors for abnormal cervical cytology. Variables Marital status Single Married Divorced Socioeconomic class Low High Educational level Primary Secondary Tertiary Past history of STI Multiple sexual partners Early coitarche (b20 y) Consistent condom use Combined oral contraceptives Early marriage (b20 y) Knowledge of pap smear Previous pap smear

HIV-negative, no. (%)

HIV-positive, no. (%)

126 (50.4) 124 (49.6) 0

64 (25.6) 186 (74.4) 0

185 (74.0) 65 (26.0)

156 (62.4) 94 (37.6)

48 (19.2) 114 (45.6) 88 (35.2) 68 (27.2) 230 (92) 185 (74) 40 (16) 30 (12) 34 (13.6) 50 (20) 2 (0.8)

36 (14.4) 78 (31.2) 136 (54.4) 36 (14.4) 186 (74.4) 144 (57.6) 26 (10.4) 38 (15.2) 56 (22.4) 84 (33.6) 4 (1.6)

P value

0.005

b0.001 b0.001 0.0001 0.06 0.29 0.3 b0.001 0.68

Table 4 CD4 count and prevalence of abnormal cytology among HIV-positive women. CD4 count, cells/mm3

Number of women (% of total)

Normal smears, no. (% of CD4 count group)

Abnormal smears, no. (% CD4 count group)

b200a 200–499a ≥500 Total

68 (27.5) 116 (47.0) 63 (25.5) 247 (100)

45 (66.2) 69 (59.5) 48 (76.2) 162

23 (33.8) 47 (40.5) 15 (23.8) 85

a

One Pap smear in the CD4 b200 group, and 2 in the 200–499 group were unsatisfactory and therefore excluded from the analysis.

compared with HIV-negative women of similar ages might imply that HIV-positive women not only are at risk of developing abnormal cervical cytology at a younger age but are also at risk of rapid progression of the disease to high-grade lesions. The present study showed that immunosuppression (CD4 count b500 cells/mm3) was significantly associated with the development of abnormal cervical cytology; however, the degree of immunosuppression might not affect the rate of progression of the disease because the incidence of HGSIL was not significantly higher among women with a CD4 count of less than 500 cells/mm3 than among those with a higher count. This is similar to the findings of Cardillo et al. [23]. Across both groups, the proportion of women who had knowledge of Pap smear (26.8%) and had had a previous Pap test (1.2%) was very low. The fact that the present study was carried out in a tertiary health institution where this service is offered, and that most of these women, especially those who were HIV-positive, were in regular contact with the health facility implies that medical personnel are not doing enough to create awareness of this preventable disease. The high cost of a Pap smear at 4000 naira (US $25) might also explain the wide disparity between knowledge and uptake of smears, because most Nigerians live on less than US $1 per day. Subsidizing the cost of Pap smear would improve its uptake by Nigerian women. As noted by Chukwuali et al. [24] in a highly subsidized center in Enugu, however, psychosocial problems might be another reason for the poor uptake of Pap smears among Nigerian women. In the absence of a national policy for cervical cancer screening, opportunistic screening remains the only hope of reducing the menace of cervical cancer in our locality in the interim. Therefore, all healthcare providers must seize every opportunity available to educate Nigerian women on cervical cancer and its prevention. As suggested by Dim et al. [25], including discussions on Pap smear and cervical cancer during post-test counseling for HIV-positive women might increase the awareness of Pap smear testing and its utilization among HIV-positive women, and such a policy should be implemented in Nigerian hospitals. Educating young girls and women on the problems of premarital sex, early initiation of sexual activity, poor utilization of condoms, and multiple sexual partners might assist in reducing the prevalence of the risk factors for abnormal cervical cytology observed in the study

Table 5 Relationship between CD4 count and grade of abnormal cervical cytology among HIV-positive women. CD4 count, cells/mm3

LGSILa

ASC-USa

HGSILa

AGC-USa

Total

b200 200–499 ≥500 Total

14 (60.9) 20 (42.6) 4 (26.7) 38

4 (17.4) 15 (31.9) 5 (33.3) 24

5 (21.7) 10 (21.3) 5 (33.3) 20

0 2 (4.3) 1 (6.7) 3

23 47 15 85

Abbreviations: AGC-US, atypical glandular cells of undetermined significance; ASC-US, atypical squamous cells of undetermined significance; HGSIL, high-grade squamous intraepithelial lesions; LGSIL, low-grade squamous intraepithelial lesions. a Values are given as number (percentage of abnormal smears in CD4 count group).

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population. In addition, a considerable number of the present study participants were of low socioeconomic status; thus, empowering the women economically and offering free education might contribute positively to reducing the prevalence of cervical dysplasia and thus cervical cancer in this environment. In summary, women with HIV infection were found to be at increased risk of abnormal cervical cytology and high-grade lesions compared with HIV-negative women. Knowledge and utilization of Pap smear were very low among the study population. HIV counseling should include discussions on cervical cancer screening, and screening for cervical cancer should be part of the routine investigations for HIV-positive women. The government should formulate and implement a national policy on cervical cancer screening, and screening should be free or highly subsidized. Conflict of interest The authors have no conflicts of interest. References [1] Onah HE, Ezugwu OF, Eze JN. Cervical cancer screening: a survey of current practice amongst Nigerian Gynaecologists. Trop J Obstet Gynaecol 2001;18(2):78–81. [2] Feyi-Wobosa AP, Kamanu C, Aluka C. Awareness and risk factors for cervical cancer among women in Aba, South-Eastern Nigeria. Trop J Obstet Gynaecol 2005;22(1):25–6. [3] van Bogaert LJ. The impact of human immunodeficiency virus infection on cervical preinvasive and invasive neoplasia in South Africa. Ecancermedicalscience 2013;7:334. [4] Isaakidis P, Pimple S, Varghese B, Khan S, Mansoor H, Ladomirska J, et al. HPV infection, cervical abnormalities, and cancer in HIV-infected women in Mumbai, India: 12-month follow-up. Int J Womens Health 2013;5:487–94. [5] Hoppenot C, Stampler K, Dunton C. Cervical cancer screening in high- and lowresource countries: implications and new developments. Obstet Gynecol Surv 2012;67(10):658–67. [6] Adewole IF, Benedet JL, Crain BT, Follen M. Evolving a strategic approach to cervical cancer control in Africa. Gynecol Oncol 2005;99(3 Suppl. 1):S209–12. [7] Olaniyan OB, Agbogoroma OC, Ladipo OP. Knowledge and practice of cervical screening among female health workers in a government hospital in Abuja metropolis, Nigeria. Trop J Obstet Gynaecol 2000;17(1):18–20.

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Abnormal cervical cytology among HIV-positive women in Nigeria.

To determine the prevalence of abnormal cervical smears and high-grade lesions among HIV-positive and HIV-negative women, and to assess the relationsh...
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