Home Print this page Email this page Small font sizeDefault font sizeIncrease font size
Users Online: 1188

 

Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Advertise Contacts Login 
     

  Table of Contents  
ORIGINAL ARTICLE
Year : 2013  |  Volume : 54  |  Issue : 3  |  Page : 176-184  

Integrating cervical cancer screening with HIV care in a district hospital in Abuja, Nigeria


1 Department of Prevention, Care and Treatment, FHI 360, Garki, Nigeria
2 Department of Family Medicine, Medical University of Southern Africa; FHI 360 South Africa, Hatfield, Pretoria, South Africa
3 Target State High Impact Project, Bauchi, Nigeria
4 Department of Obstetrics and Gynaecology, Maitama District Hospital, Abuja, Nigeria
5 HIV/AIDS/TB Unit, USAID Nigeria, Maitama, Abuja, Nigeria

Date of Web Publication5-Jul-2013

Correspondence Address:
Solomon Odafe
Department of Prevention, Care and Treatment FHI360, Plot 1071 J.S Tarka Street Abuja
Nigeria
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0300-1652.114590

Rights and Permissions
   Abstract 

Background: Human immunodeficiency virus positive (HIV+) women have a higher risk of developing invasive cervical cancer compared with uninfected women. This study aims to document programmatic experience of integrating cervical cancer screening using Visual Inspection and Acetic Acid (VIA) into HIV care as well as to describe patients' characteristics associated with positive VIA findings amongst HIV+ women. Materials and Methods: A cross-sectional study analysed routine service data collected at the antiretroviral therapy (ART) and cervical cancer screening services. Our program integrated screening for cervical cancer using VIA technique to HIV care and treatment services through a combination of stakeholder engagement, capacity building for health workers, creating a bi-directional referral between HIV and reproductive health (RH) services and provider initiated counselling and screening for cervical cancer. Information on patients' baseline and clinical characteristics were captured using an electronic medical records system and then exported to Statistical Package for the Social Sciences (SPSS). Logistic regression model was used to estimate factors that influence VIA results. Results: A total of 834 HIV+ women were offered VIA screening between April 2010 and April 2011, and 805 (96.5%) accepted it. Complete data was available for 802 (96.2%) women. The mean age at screening and first sexual contact were 32.0 (SD 6.6) and 18.8 (SD 3.5) years, respectively. VIA was positive in 52 (6.5%) women while 199 (24.8%) had a sexually transmitted infection (STI). Of the 199 who had a STI, eight (4.0%) had genital ulcer syndrome, 30 (15.1%) had lower abdominal pain syndrome and 161 (80.9%) had vaginal discharge syndrome. Presence of lower abdominal pain syndrome was found to be a significant predictor of a positive VIA result ( P = 0.001). Women with lower abdominal pain syndrome appeared to be more likely (OR 47.9, 95% CI: 4.8-480.4, P = 0.001) to have a positive VIA result. Conclusion: The high burden of both HIV and cervical cancer in developing countries makes it a necessity for integrating services that offer early detection and treatment for both diseases. The findings from our study suggest that integrating VIA screening into the package of care offered to HIV+ women is feasible and acceptable.

Keywords: Cervical cancer screening, human immunodeficiency virus, integration, Nigeria, visual inspection with acetic acid


How to cite this article:
Odafe S, Torpey K, Khamofu H, Oladele E, Adedokun O, Chabikuli O, Mukaddas H, Usman Y, Aiyenigba B, Okoye M. Integrating cervical cancer screening with HIV care in a district hospital in Abuja, Nigeria. Niger Med J 2013;54:176-84

How to cite this URL:
Odafe S, Torpey K, Khamofu H, Oladele E, Adedokun O, Chabikuli O, Mukaddas H, Usman Y, Aiyenigba B, Okoye M. Integrating cervical cancer screening with HIV care in a district hospital in Abuja, Nigeria. Niger Med J [serial online] 2013 [cited 2019 Nov 19];54:176-84. Available from: http://www.nigeriamedj.com/text.asp?2013/54/3/176/114590


   Introduction Top


In sub-Saharan Africa, women account for about 60% of people living with human immunodeficiency virus (HIV) [1] , and young women aged 15-24 years are as much as eight times more likely than men to be HIV positive (HIV+). [2] Cervical cancer is the second most common type of cancer amongst women worldwide. [3] Human papilloma virus (HPV) is the primary etiologic agent of cervical cancer. [4],[5] Globally, HPV types 16 and 18, both of which are vaccine-preventable types, contribute to more than 70% of all cervical cancer cases. [6] HPV-16 and 18, also contribute between 41% and 67% of high-grade and 16-32% of low-grade cervical lesions. [6] Transmission of HPV occurs primarily by sexual contact. [4],[7],[8] Known predisposing factors for HPV infection and later cervical cancer include early age at first sexual intercourse, multiple sexual partners, a male spouse who has had intercourse with multiple women, smoking and women who are immunosuppressed. [7],[8],[9],[10]

About 83% of new cases of cervical cancer and 85% of associated mortality occur in developing countries. [3] Low perception of risks and lack of awareness about cervical cancer screening amongst women and challenges of access to cervical cancer screening for early detection of disease have been reported amongst factors responsible for increasing incidence and mortality due to cervical cancer in developing countries. [11],[12],[13],[14],[15] A four- to six-fold increased risk for squamous intraepithelial lesions (SIL) or cervical intraepithelial neoplasia (CIN) is estimated in HIV+ women compared with negative women. [16],[17],[18],[19],[20] HIV+ women are also more likely to have cervical abnormalities that can progressively lead to invasive cervical cancer. [21],[22],[23],[24] Cervical cancer incidence and related mortality have decreased in developed countries due mainly to regular screening and prompt treatment for sexually active women. [25] HIV treatment recommendations advise that a woman who is diagnosed with HIV should also be screened for cervical cancer. [26]

Several African countries have used cytologic screening to screen for cervical cancer among HIV+ women; studies on these programs reported that 55-76% of HIV+ women had an abnormal  Pap smear More Details. [27],[28],[29] Early detection of potentially cancerous cervical cell changes provides the best opportunity for effective treatment. However, access to screening and treatment for cervical cancer in Sub-Sahara Africa [30] and Nigeria in particular is limited. [13] A recent review estimated that rates of cervical screening coverage in sub-Saharan Africa in general range from 2% to 20.2% in urban areas and 0.4% to 14% in rural areas. [31] Challenges to the provision of cervical cancer screening include poor infrastructural facilities, lack of skilled human resources, lack of commodities needed to carry out screening, and low levels of awareness amongst patients and health workers. [11],[14],[32],[33],[34] Cervical cancer screening messages are also not part of routine HIV counselling in many Nigerian clinics. [12]

Various attempts at improving cervical cancer screening in developing countries have been made. [35] Different screening methods have also been evaluated. [35] The cost of deploying cytology-based screening, followed by colposcopy, is not suitable for widespread scale up of cervical cancer screening in many developing countries. However, techniques such as visual inspection with acetic acid (VIA) and visual inspection with Lugol's Iodine (VILI) are less expensive and require minimal supplies and infrastructure. [36] The U.S. Centre for Disease Control and Prevention (CDC) has funded programs that recorded demonstrable success in using VIA for cervical cancer screening, through advocacy and capacity building in Kenya, Bolivia, and India. [37] In Peru, VIA was found to be useful for detection of precursor lesions of cervical cancer not only in low-resource settings but also in well-equipped health centres and cancer centres. [38] Its positive predictive value was comparable to the conventional Pap smear. [38] VIA was found to be more likely to achieve earlier diagnosis, follow-up, and treatment than cytology based screening. [38] VIA in screening for cervical cancer has also been successfully used in Nigeria and Zambia and other developing countries and has been found to compare favourably with cytology. [39],[40],[41],[42],[43],[44]

There is an increasing focus on ensuring that the gains of antiretroviral therapy (ART) are sustained through prevention of other causes of morbidity and mortality in those living with HIV. Nonetheless screening for cervical cancer in Nigeria remains poor. [13] In an effort to address this gap, Family Health International (FHI) 360 launched a pilot program to integrate cervical cancer screening services using VIA for HIV+ women attending the ART clinic in a public health facility in Abuja, Nigeria. This paper aims to document programmatic experience of integrating VIA screening into HIV care as well as to describe patients' characteristics associated with positive VIA findings among the HIV+ women who participated in the pilot.


   Materials and Methods Top


This was a cross-sectional study using linked routine service data collected at the ART and cervical cancer screening service delivery points between April 2010 and April 2011.

The study was conducted in Maitama District Hospital (MDH), a government-owned 93 bed secondary healthcare public hospital that provides comprehensive HIV/AIDS prevention, care and treatment services in the Abuja metropolis in Nigeria. The hospital was one of the sites supported by Global HIV/AIDS Initiative Nigeria (GHAIN) project through funding from the United States Agency for International Development (USAID) under the United States President's Emergency Plan for AIDS Relief (PEPFAR). FHI 360 piloted the integration of cervical cancer screening using VIA technique in this hospital over a 1-year-period from April 2010 and April 2011.

Considerations for choosing a site for this pilot were: 1) Presence of a comprehensive HIV treatment program; 2) presence of a reproductive health unit that can be supported to provide VIA; 3) presence of an Electronic Medical Records (EMR) system and 4) a high patient load (average general outpatient attendance of over 1,000/month). The Maitama District Hospital (MDH) was chosen for this pilot because it met all the above criteria.

This study focussed on adult female patients in the reproductive age group (20-49 years). Women with a total hysterectomy, history of cervical cancer, or current pregnancy were excluded from the study. All other women aged 20-49 years either newly diagnosed of HIV or with known HIV+ on ART who accepted VIA screening for cervical cancer between April 2010 and April 2011 at MDH constitute the study population.

The integration process was preceded by advocacy meetings and enlisting of support of various stakeholders followed by a site assessment. Data from an EMR system developed by FHI 360, the Lafiya Management Information System (LAMIS ® ) were reviewed to ascertain the number of HIV+ women meeting selection criteria enrolled in the ART program. The reproductive health (RH) and ART units were assessed to determine infrastructure, basic equipment and supplies, and training needs for the pilot program. Nurses/midwives at the reproductive health unit were trained during a 2-day intensive course on-site on use of the VIA technique, using the practical manual on visual screening for cervical neoplasia published by World Health Organization (WHO)-International Agency for Research on Cancer (IARC). [45] Trainings were conducted by a gynaecologist and FHI technical staff experienced on use of the VIA technique. Additional training included practical sessions at clinics and review of pictures of normal and abnormal cervix. Additionally, refresher trainings were provided during the pilot. The implementation process was supervised daily by an experienced gynaecologist and FHI technical staff to ensure quality of screening process.

Furthermore, relevant supplies required for VIA screening were provided. Nurses/midwives at both the ART and RH units were also trained on counselling, appointment setting and a bi-directional referral and patient tracking system were established. Messages on cervical cancer prevention and importance of screening were introduced as part of health talks delivered to patients in the ART clinic. During implementation, women attending the ART clinic were counselled on cervical cancer screening, and patients accepting to test were subsequently referred to the RH unit for a same-day screening using the VIA technique.

At the RH unit, women participated in a group education session. Subsequently, women were individually counselled and provided their consent. The trained nurses/midwifes then completed patients' information on the cervical cancer screening form. To begin the screening, a midwife performed abdominal and external genitalia examinations, a Graves' speculum was inserted, and the cervix was brought into view. The midwife then examined the cervix using an examination light and identified the squamocolumnar junction (SCJ). The cervix was then assessed for the presence of gross lesions consistent with possible cancer. After cleaning out excess mucus using a cotton swab, a dilute (5%) acetic acid solution was applied liberally to the cervix. After waiting for 1 min, the cervix was re-examined for lesions. Midwifes were trained to ensure that the entire SCJ was visualised. Assessment findings were recorded with three standardised VIA categories. [45] The VIA test outcome were classified as negative, positive or indicative using the classifications described in the IARC training manual [45] and appropriately recorded on a cervical cancer screening data collection form after each screening procedure. VIA positive test outcome includes the presence of distinct, well-defined, dense acetowhite areas with regular or irregular margins, close to or bordering the SCJ in the transformation zone or close to the external os, if the SCJ is not visible. [45] Women with suspicious lesions were referred to a tertiary centre for colposcopy and treatment. The VIA service at MDH was offered free of charge, however, patients referred to the tertiary center for confirmatory testing and possible treatment were required to pay for services rendered.

Routine service data from the VIA screening process and ART services were collected at the program monitoring unit, ART clinic and cervical cancer screening unit. A cervical screening data collection form capturing patients ART unique identification number and outcome of screening, was specifically developed for collecting data at the VIA screening point. LAMIS was used to capture linked patients' information on demographic, including age, age at first sexual contact, marital status, and level of education. Information on baseline clinical characteristics obtained included weight, CD4 count and WHO staging.

Data analysis

The data were exported from LAMIS to SPSS for statistical analysis. Patients' personal identifiers were removed at the point of data export. Automated and manual consistency checks were performed on the data. In instances where inconsistencies were found in the EMR, data inconsistencies were corrected using source documents. A logistic regression model was used for univariate and multivariate analyses of the association between the outcome of the VIA test (i.e., positive and negative) and patients' characteristics. All statistical tests were two-sided at α = 0.05.

Ethical considerations

Ethical approval was obtained from the Nigerian National Health and Research Ethics Committee (NHREC) and FHI's Protection of Human Subjects Committee (PHSC). In addition, data entry clerks were trained on confidentiality. Secure data entry, transmission and storage were ensured. Patients who accepted to be screened for cervical cancer were further required to give verbal consent before the screening was performed, as part of the ethical requirements.


   Results Top


Eight hundred and thirty-four HIV+ women on ART were offered VIA screening between April 2010 and April 2011. Eight hundred and five (96.5%) of these women accepted screening and complete records were available for 802 (96.2%) of them. The mean age of those women with complete records was 32.0 (SD 6.6) years. Nearly half of the study population (47.4%, n = 380) had secondary education, about one third (29.5%, n = 237) had tertiary education, 15.1% (n = 121) had primary education, 5.7% (n = 46) had no formal education, and the level of education was not stated for 2.2% (n = 18) women. Married women accounted for 56.1% (n = 451) of the study population, while 29.4% (n = 237) were single, 13.4% (n = 106) were either divorced or widowed, and 1.0% (n = 8) did not have a marital status recorded. The mean age at first sexual contact was 18.8 (SD 3.5) years. [Table 1] summarizes baseline characteristics of study population.
Table 1: Baseline characteristics of respondents


Click here to view


Complete baseline CD4 count records were available for 495 (61.7%) of women screened. Clinical records showed that 287 (35.8%) of the women screened had baseline CD4 counts <200 cells/μl, 186 (23.2%) had counts between 200-350 cells/μl, and 22 (2.7%) had CD4 count >350 cells/μl. HIV clinical staging at baseline was recorded for only 535 (66.7%) of women screened, of which 235 were in WHO stage I, 144 women were at stage II, 150 women stage III, and six of them had stage IV disease.

Unaided visual inspection revealed a healthy cervix in 543 (67.7%) of women, redness in 51 (6.4%), Nabothian follicles in 49 (6.1%), while the results for unaided visual inspection were not documented for 159 (19.8%). Visual inspection with acetic acid was positive in 52 (6.5%) women. All the women were also screened for STI using symptom checklist and 199 (24.8%) had a STI syndrome. Of the 199 women, who had an STI syndrome, eight (4.0%) had genital ulcer syndrome, 30 (15.1%) had lower abdominal pain syndrome and 161 (80.9%) had vaginal discharge syndrome. [Table 2] summarizes the findings from clinical consultation and VIA screening. [Figure 1] summarizes cervical cancer screening patient flow.
Table 2: Findings from clinical consultations and screening


Click here to view
Figure 1: Cervical cancer (VIA) screening flow chart

Click here to view


The mean patients' age and age at first sexual contact were not associated with a positive VIA result (P = 0.669 and P = 0.876 respectively). A statistically significant association was observed for positive VIA results and having STI syndrome (P = 0.001). However, no statistically significant associations were observed for: Positive VIA results and HIV clinical staging at baseline (P = 0.999); level of education (P = 0.157); marital status (P = 0.546) and CD4 count values (P = 0.279). [Table 3] summarizes factors associated with a positive VIA result. The results from the regression model showed that after controlling for the effect of other factors, having lower abdominal pain syndrome was found to significantly predict a positive VIA result (P = 0.001). Women with lower abdominal pain syndrome in this study were more likely to have a positive VIA result (OR 47.9, 95% CI: 4.8-480.4, P = 0.001).
Table 3: Factors influencing a positive VIA result (logistic regression)


Click here to view



   Discussion Top


The results obtained in this study appear to indicate that demographic and baseline clinical characteristics such as age, weight, CD4 count, and WHO staging were not significantly associated with positive VIA results amongst HIV positive women on ART. However, lower abdominal pain syndrome was a significant predictor of positive VIA result. This finding is consistent with findings reported in another study in Nigeria that found higher incidence of cervical dysplasia amongst patients with chronic pelvic inflammatory disease. [46] Findings from another study in the United States suggested that coexistent of pelvic infection in HIV+ women may contribute to development and spread of cervical cancer. [47]

In our study, 96.5% of women offered screening for cervical cancer accepted testing. This finding was comparable with findings from studies in Kenya and Mozambique that reported acceptance rates of 87% and 86%, respectively, of cervical cancer screening using VIA technique. [48],[49] Though level of patients' satisfaction with the VIA screening provided was not specifically assessed in this study, in a similar study in Thailand, over 95% of women expressed satisfaction with their experience with visual inspection test. [50] This finding indicated that majority of women will accept screening for cervical cancer, if offered the opportunity to test.

There appear to be conflicting evidence, based on previously published data, regarding the influence of clinical characteristics and ART on Human Papilloma Virus (HPV) infection, and the development of intraepithelial neoplasia. [16],[27],[51],[52],[53],[54] For example, an analysis of 1639 HIV+ and 452 HIV negative women in a study in the United States showed that abnormal cytology progression was significantly increased only among the most immunosuppressed women, while regression was significantly reduced in all HIV seropositive women except those with the best controlled HIV disease. [16] In this study, however, there was no statistically significant association observed between CD4 count values and the occurrence of cervical neoplasia, which was consistent with findings reported by some studies. [55],[56]

The incidence rates of cervical cancer have been reported to vary with geographical region. [57],[58] The Eastern African region followed by the western region, then South African region have been reported to have the highest age-standardised incidence of cervical cancer in the African continent. [6],[59] These regional differences might be explained by genetic variations, differences in lifestyles, environmental factors and medical practices such as screening which are important determinants of cancer risk. [60] This assumption is reinforced by migration patterns that show that incidence of cancer among migrant's changes to more closely reflect the rates in the adoptive country. [60],[61] Hence, reported positivity rates with VIA also vary by country and region. A study in Côte d'Ivoire reported a rate VIA positivity rate of 9.0% amongst HIV+ women and 3.9% amongst HIV negative women. [36] A similar study in Kenya amongst women in HIV care reported a positivity rate of 7.1%. [48] Studies have also reported comparatively lower VIA positivity rates amongst HIV negative women. [36],[62] Our pilot program indicated a positive VIA result of 6.4% amongst HIV+ women on ART. Our finding was comparable with the 7.7% and 7.1% VIA positivity rate observed in studies in Kenya and Bangladesh. [48],[63] The lower positivity observed in our study could be ascribed to the fact that all HIV+ women screened in our program were already on ART. Studies have suggested that ART may decrease the risk of cervical cancer in HIV+ women. [64],[65],[66]

Our study could not compare positive VIA result with colposcopy and histology findings because the majority of patients did not receive colposcopy and histology. While we cannot determine the true performance of VIA screening in our context, there is evidence in the literature on the positive predictive value, sensitivity and specificity of VIA. A study in Bangladesh that compared Pap smear and VIA outcomes with histology results of tissues obtained from colposcopy directed biopsy revealed that VIA had a 94.4% sensitivity rate compared with 55.5% observed with pap smear. [63] Another study reported specificity and sensitivity rates of 82.5% and 66.9%, respectively, with VIA compared with 77.5% and 86.8%, respectively, with Pap smear in low resource settings. [67] Additional evidence on the positive predictive value (PPV), reported a PPV of 26.7% for Pap smear and 7.1% for VIA. [68]

Our pilot program integrated screening for cervical cancer using VIA technique into HIV care and treatment program in MDH through a combination of stakeholder engagement, capacity building for health workers, creating a bi-directional referral between HIV and RH services, and provision of the required commodities and equipment. The program highlighted several lessons and identified an important challenge. First, integration of cervical cancer screening and ART services in resource-limited settings is possible, and second, the majority of HIV+ women would agree to screening for cervical cancer if offered and provided free of cost. However, the inability of the majority of patients to afford the required confirmation investigations was a considerable challenge.

We observed that out of a total of 52 VIA positive women, 35 (67.3%) could not access further care at the tertiary site due to cost. Patients' inability to pay for follow up investigations also accounted for significant losses in a similar study in Côte d'Ivoire. [36] Other programs that used a test and treat approach recorded better uptake of confirmatory test and treatment. [48],[63],[69] The significant losses observed in our study with an approach that refers patient for confirmation and treatment suggest that a "test and treat" approach that combines colposcopy, biopsy and immediate cryotherapy for positively screened cervical lesions in one site may provide better outcomes. However, considering the fact the majority of women in Nigeria access care in primary health centres were 'screen and refer' services maybe the only feasible option, providing free or subsidized treatment services at referral centres after screening is likely to significantly increase uptake.

Lastly, our study results should be interpreted with caution, as information on patients' clinical characteristics such as CD4 count and WHO staging were obtained from patient records entered into the LAMIS and were therefore subject to availability of data. Complete patient record for CD4 count and WHO staging were available for 61.7% and 66.7% of patients, respectively. Additionally, in our study, because the majority of women with positive VIA did not access colposcopy and histology sampling, we could not evaluate the performance of the visual inspection test in our study population.


   Conclusion Top


The high burden of both HIV and cervical cancer in developing countries makes it a necessity for integrating services that offer early detection and treatment for both diseases. Our study findings suggest that integrating VIA screening into the package of care offered to HIV+ women is feasible and acceptable. Positive VIA test was associated with presence of a lower abdominal pain syndrome. Cervical cancer screening should be included as a standard package of care in HIV treatment programs. However, an approach that combines confirmation of lesions and treatment may reduce losses and improve outcomes.


   Acknowledgments Top


We gratefully acknowledge the contributions of Dr. Tim Efuntoye and the Federal Capital Territory (FCT) Abuja GHAIN team that provided technical support to the health facility where this program was implemented. The technical support of both the HIV and AIDS Division of the Federal Ministry of Health and the National AIDS Control Agency in Nigeria were vital in the successful implementation of this pilot program. We also acknowledge Rebecca Dirks of FHI360 Washington DC for her review and contributions to this manuscript. Support for this paper was provided by FHI360's Global HIV/AIDS Initiative in Nigeria with funds from the U.S. President's Emergency Plan for AIDS Relief (PEPFAR) through U.S. Agency for International Development (USAID) Cooperative Agreement No. 620-A-00-04-00122-00. The views expressed in this publication do not necessarily reflect those of FHI360, nor the United States Government.

 
   References Top

1.UNAIDS. Sub-Sahara Africa, AIDS Epidemic update. Geneva: UNAIDS; Nov. 2009; p. 21-2. Available from: http://www.unaids.org/en/media/unaids/contentassets/dataimport/pub/report/2009/jc1700_epi_update_2009_en.pdf.[Last accessed on 2012 June 8].  Back to cited text no. 1
    
2.UNAIDS. Report on the global AIDS epidemic. Geneva: WHO; 2010; p. 10. Available from: http://www.unaids.org/documents/20101123_globalreport_em.pdf. [Last accessed on 2012 June 8].  Back to cited text no. 2
    
3.Anorlu RI. Cervical cancer: The sub-Saharan African perspective. Reprod Health Matters 2008;16:41-9.  Back to cited text no. 3
[PUBMED]    
4.Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah VK, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348:518-27.  Back to cited text no. 4
    
5.Anorlu RI. What is the significance of the HPV epidemic? Can J Urol 2008;15:3860-5.  Back to cited text no. 5
[PUBMED]    
6.WHO/Institut Catala d'Oncologia (ICO). Human Papillomavirus and Related Cancers (Summary report update). In: WHO/ICO Information centre, editor. Geneva: WHO; Nov. 2010. Available from: http://apps.who.int/hpvcentre/statistics/dynamic/ico/country_pdf/XWX.pdf. [Last accessed on 2013 Feb].  Back to cited text no. 6
    
7.Oakeshott P, Aghaizu A, Reid F, Howell-Jones R, Hay PE, Sadiq ST, et al. Frequency and risk factors for prevalent, incident, and persistent genital carcinogenic human papillomavirus infection in sexually active women: Community based cohort study. BMJ 2012;344:e4168.  Back to cited text no. 7
[PUBMED]    
8.Hendricks KA. Re: "Genital human papillomavirus infection: Iincidence and risk factors in a cohort of female university students". Am J Epidemiol 2003;158:927.  Back to cited text no. 8
[PUBMED]    
9.Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF, et al. Genital human papillomavirus infection in men: Incidence and risk factors in a cohort of university students. J Infect Dis 2007;196:1128-36.  Back to cited text no. 9
[PUBMED]    
10.Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA. Genital human papillomavirus infection: Incidence and risk factors in a cohort of female university students. Am J Epidemiol 2003;157:218-26.  Back to cited text no. 10
[PUBMED]    
11.Ayinde OA, Omigbodun AO, Ilesanmi AO. Awareness of cervical cancer, Papanicolaou's smear and its utilisation among female undergraduates in Ibadan. Afr J Reprod Health 2004;8:68-80.  Back to cited text no. 11
[PUBMED]    
12.Dim CC, Dim NR, Ezegwui HU, Ikeme AC. An unmet cancer screening need of HIV-positive women in southeastern Nigeria. Medscape J Med 2009;11:19.  Back to cited text no. 12
[PUBMED]    
13.Dim CC, Nwagha UI, Ezegwui HU, Dim NR. The need to incorporate routine cervical cancer counselling and screening in the management of women at the outpatient clinics in Nigeria. J Obstet Gynaecol 2009;29:754-6.  Back to cited text no. 13
[PUBMED]    
14.Kabir M, Iliyasu Z, Abubakar IS, Mahboob S. Awareness and practice of cervical cancer screening among female health professionals in Murtala Mohammed Specialist Hospital, Kano. Niger Postgrad Med J 2005;12:179-82.  Back to cited text no. 14
[PUBMED]    
15.Ezechi OC, Gab-Okafor CV, Ostergren PO, Odberg Pettersson K. Willingness and acceptability of cervical cancer screening among HIV positive Nigerian women. BMC Public Health 2013;13:46.  Back to cited text no. 15
[PUBMED]    
16.Massad LS, Ahdieh L, Benning L, Minkoff H, Greenblatt RM, Watts H, Miotti P, et al. Evolution of cervical abnormalities among women with HIV-1: Evidence from surveillance cytology in the women's interagency HIV study. J Acquir Immune Defic Syndr 2001;27:432-42.  Back to cited text no. 16
[PUBMED]    
17.Mandelblatt JS, Fahs M, Garibaldi K, Senie RT, Peterson HB. Association between HIV infection and cervical neoplasia: Implications for clinical care of women at risk for both conditions. AIDS 1992;6:173-8.  Back to cited text no. 17
[PUBMED]    
18.De Vuyst H, Lillo F, Broutet N, Smith JS. HIV, human papillomavirus, and cervical neoplasia and cancer in the era of highly active antiretroviral therapy. Eur J Cancer Prev 2008;17:545-54.  Back to cited text no. 18
[PUBMED]    
19.Ellerbrock TV, Chiasson MA, Bush TJ, Sun XW, Sawo D, Brudney K, et al. Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA 2000;283:1031-7.  Back to cited text no. 19
[PUBMED]    
20.Moscicki AB, Ellenberg JH, Crowley-Nowick P, Darragh TM, Xu J, Fahrat S. Risk of high-grade squamous intraepithelial lesion in HIV-infected adolescents. J Infect Dis 2004;190:1413-21.  Back to cited text no. 20
[PUBMED]    
21.Holschneider CH. Premalignant and malignant disorders of the uterine cervix. In: Alan HD, Lauren N, editors. Current Obstetrics and Gynecologic Diagnosis and Treatment. 9 th ed. New York: McGraw-Hill; 2003. p. 894-916.  Back to cited text no. 21
    
22.Frisch M, Biggar RJ, Goedert JJ. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst 2000;92:1500-10.  Back to cited text no. 22
[PUBMED]    
23.Dal Maso L, Franceschi S, Polesel J, Braga C, Piselli P, Crocetti E, et al. Risk of cancer in persons with AIDS in Italy, 1985-1998. Br J Cancer 2003;89:94-100.  Back to cited text no. 23
[PUBMED]    
24.Mbulaiteye SM, Katabira ET, Wabinga H, Parkin DM, Virgo P, Ochai R, et al. Spectrum of cancers among HIV-infected persons in Africa: The Uganda AIDS-Cancer Registry Match Study. Int J Cancer 2006;118:985-90.  Back to cited text no. 24
[PUBMED]    
25.Saslow D, Runowicz CD, Solomon D, Moscicki AB, Smith RA, Eyre HJ, et al. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin 2002;52:342-62.  Back to cited text no. 25
[PUBMED]    
26.US Department of Health and Human Services. Treatment of opportunistic infections. Available from: http://www.aidsinfo.nih.gov. Washington DC: US Department of Health and Human Services, National Institutes of Health, CDC; 2006 [Last cited on 2010 Jun 6].  Back to cited text no. 26
    
27.Denny L, Boa R, Williamson AL, Allan B, Hardie D, Stan R, et al. Human papillomavirus infection and cervical disease in human immunodeficiency virus-1-infected women. Obstet Gynecol 2008;111:1380-7.  Back to cited text no. 27
[PUBMED]    
28.Moodley JR, Constant D, Hoffman M, Salimo A, Allan B, Rybicki E, et al. Human papillomavirus prevalence, viral load and pre-cancerous lesions of the cervix in women initiating highly active antiretroviral therapy in South Africa: A cross-sectional study. BMC Cancer 2009;9:275.  Back to cited text no. 28
[PUBMED]    
29.Parham GP, Sahasrabuddhe VV, Mwanahamuntu MH, Shepherd BE, Hicks ML, Stringer EM, et al. Prevalence and predictors of squamous intraepithelial lesions of the cervix in HIV-infected women in Lusaka, Zambia. Gynecol Oncol 2006;103:1017-22.  Back to cited text no. 29
[PUBMED]    
30.Mwanahamuntu MH, Sahasrabuddhe VV, Kapambwe S, Pfaendler KS, Chibwesha C, Mkumba G, et al. Advancing cervical cancer prevention initiatives in resource-constrained settings: Insights from the Cervical Cancer Prevention Program in Zambia. PLoS Med 2011;8:e1001032.  Back to cited text no. 30
[PUBMED]    
31.Louie KS, de Sanjose S, Mayaud P. Epidemiology and prevention of human papillomavirus and cervical cancer in sub-Saharan Africa: A comprehensive review. Trop Med Int Health 2009;14:1287-302.  Back to cited text no. 31
[PUBMED]    
32.Ezem BU. Awareness and uptake of cervical cancer screening in Owerri, South-Eastern Nigeria. Ann Afr Med 2007;6:94-8.  Back to cited text no. 32
[PUBMED]  Medknow Journal  
33.Ajayi IO, Adewole IF. Knowledge and attitude of general outpatient attendants in Nigeria to cervical cancer. Cent Afr J Med 1998;44:41-3.  Back to cited text no. 33
[PUBMED]    
34.Nnodu O, Erinosho L, Jamda M, Olaniyi O, Adelaiye R, Lawson L, et al. Knowledge and attitudes towards cervical cancer and human papillomavirus: A Nigerian pilot study. Afr J Reprod Health 2010;14:95-108.  Back to cited text no. 34
[PUBMED]    
35.Arbyn M, Sankaranarayanan R, Muwonge R, Keita N, Dolo A, Mbalawa CG, et al. Pooled analysis of the accuracy of five cervical cancer screening tests assessed in eleven studies in Africa and India. Int J Cancer 2008;123:153-60.  Back to cited text no. 35
[PUBMED]    
36.Horo A, Jaquet A, Ekouevi DK, Toure B, Coffie PA, Effi B, et al. Cervical cancer screening by visual inspection in Côte d'Ivoire, operational and clinical aspects according to HIV status. BMC Public Health 2012;12:237.  Back to cited text no. 36
[PUBMED]    
37.Tesfa A. Combating cervical cancer in Ethiopia. Pathfinder Int Ethiopia April 2010. Available from: http://www.pathfinder.org/publications-tools/pdfs/Combating-Cervical-Cancer-in-Ethiopia.pdf. [Last accessed on 2012 Dec 12].  Back to cited text no. 37
    
38.Jeronimo J, Morales O, Horna J, Pariona J, Manrique J, Rubinos J, et al. Visual inspection with acetic acid for cervical cancer screening outside of low-resource settings. Rev Panam Salud Publica 2005;17:1-5.  Back to cited text no. 38
    
39.Akinwuntan AL, Adesina OA, Okolo CA, Oluwasola OA, Oladokun A, Ifemeje AA, et al. Correlation of cervical cytology and visual inspection with acetic acid in HIV-positive women. J Obstet Gynaecol 2008;28:638-41.  Back to cited text no. 39
[PUBMED]    
40.Lim K, Davidson A, Harwell J, Thay S, Boardman LA, Feller E, et al. Comparing visual inspection with acetic acid to cytology in detection of precancerous lesions of the cervix in HIV-Infected Cambodian women. J Int Assoc Physicians AIDS Care (Chic) 2011;10:283-6.  Back to cited text no. 40
[PUBMED]    
41.Mabeya H, Khozaim K, Liu T, Orango O, Chumba D, Pisharodi L, et al. Comparison of conventional cervical cytology versus visual inspection with acetic acid among human immunodeficiency virus-infected women in Western Kenya. J Low Genit Tract Dis 2012;16:92-7.  Back to cited text no. 41
[PUBMED]    
42.Pfaendler KS, Mwanahamuntu MH, Sahasrabuddhe VV, Mudenda V, Stringer JS, Parham GP. Management of cryotherapy-ineligible women in a "screen-and-treat" cervical cancer prevention program targeting HIV-infected women in Zambia: Lessons from the field. Gynecol Oncol 2008;110:402-7.  Back to cited text no. 42
[PUBMED]    
43.Ramogola-Masire D, de Klerk R, Monare B, Ratshaa B, Friedman HM, Zetola NM. Cervical cancer prevention in HIV-infected women using the "see and treat" approach in Botswana. J Acquir Immune Defic Syndr 2012;59:308-13.  Back to cited text no. 43
[PUBMED]    
44.Sahasrabuddhe VV, Bhosale RA, Kavatkar AN, Nagwanshi CA, Joshi SN, Jenkins CA, et al. Comparison of visual inspection with acetic acid and cervical cytology to detect high-grade cervical neoplasia among HIV-infected women in India. Int J Cancer 2012;130:234-40.  Back to cited text no. 44
[PUBMED]    
45.Sankaranarayanan R, Wesley RS. A Practical Manual on Visual Screening for Cervical Neoplasia. Lyon: Technical Publication No 41, IARC Press; 2003; p. 15-27. Available from: http://screening.iarc.fr/doc/viavilimanual.pdf. [Last accessed on 2010 Jan 23].  Back to cited text no. 45
    
46.Abdul MA, Shittu SO, Randawa JA, Shehu MS. The cervical smear pattern in patients with chronic pelvic inflammatory disease. Niger J Clin Pract 2009;12:289-93.  Back to cited text no. 46
[PUBMED]    
47.Singh GS, Aikins JK, Deger R, King S, Mikuta JJ. Metastatic cervical cancer and pelvic inflammatory disease in an AIDS patient. Gynecol Oncol 1994;54:372-6.  Back to cited text no. 47
[PUBMED]    
48.Huchko MJ, Bukusi EA, Cohen CR. Building capacity for cervical cancer screening in outpatient HIV clinics in the Nyanza province of western Kenya. Int J Gynaecol Obstet 2011;114:106-10.  Back to cited text no. 48
[PUBMED]    
49.Audet CM, Silva Matos C, Blevins M, Cardoso A, Moon TD, Sidat M. Acceptability of cervical cancer screening in rural Mozambique. Health Educ Res 2012;27:544-51.  Back to cited text no. 49
    
50.Gaffikin L, Blumenthal PD, Emerson M, Limpaphayom K. Royal Thai College of Obstetricians and Gynaecologists (RTCOG)/JHPIEGO Corporation Cervical Cancer Prevention Group. Safety, acceptability, and feasibility of a single-visit approach to cervical-cancer prevention in rural Thailand: A demonstration project. Lancet 2003;361:814-20.  Back to cited text no. 50
    
51.Palefsky JM, Minkoff H, Kalish LA, Levine A, Sacks HS, Garcia P, et al. Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. J Natl Cancer Inst 1999;91:226-36.  Back to cited text no. 51
[PUBMED]    
52.Ahdieh L, Munoz A, Vlahov D, Trimble CL, Timpson LA, Shah K. Cervical neoplasia and repeated positivity of human papillomavirus infection in human immunodeficiency virus-seropositive and seronegative women. Am J Epidemiol 2000;151:1148-57.  Back to cited text no. 52
    
53.Ahdieh-Grant L, Li R, Levine AM, Massad LS, Strickler HD, Minkoff H, et al. Highly active antiretroviral therapy and cervical squamous intraepithelial lesions in human immunodeficiency virus-positive women. J Natl Cancer Inst 2004;96:1070-6.  Back to cited text no. 53
[PUBMED]    
54.Paramsothy P, Jamieson DJ, Heilig CM, Schuman PC, Klein RS, Shah KV, et al. The effect of highly active antiretroviral therapy on human papillomavirus clearance and cervical cytology. Obstet Gynecol 2009;113:26-31.  Back to cited text no. 54
[PUBMED]    
55.Lillo FB, Ferrari D, Veglia F, Origoni M, Grasso MA, Lodini S, et al. Human papillomavirus infection and associated cervical disease in human immunodeficiency virus-infected women: Effect of highly active antiretroviral therapy. J Infect Dis 2001;184:547-51.  Back to cited text no. 55
[PUBMED]    
56.Del Mistro A, Bertorelle R, Franzetti M, Cattelan A, Torrisi A, Giordani MT, et al. Antiretroviral therapy and the clinical evolution of human papillomavirus-associated genital lesions in HIV-positive women. Clin Infect Dis 2004;38:737-42.  Back to cited text no. 56
[PUBMED]    
57.Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893-917.  Back to cited text no. 57
[PUBMED]    
58.Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.  Back to cited text no. 58
[PUBMED]    
59.WHO/IARC. Cervical Cancer Incidence, Mortality and Prevalence Worldwide in 2008, Summary. Available from: http://globocan.iarc.fr/factsheet.asp. Geneva: IARC; 2008 [Last cited on 2013 Mar 21].  Back to cited text no. 59
    
60.Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev 2010;19:1893-907.  Back to cited text no. 60
    
61.Jemal A, Fedewa SA. Is the prevalence of ER-negative breast cancer in the US higher among Africa-born than US-born black women? Breast Cancer Res Treat 2012;135:867-73.  Back to cited text no. 61
[PUBMED]    
62.Keita N, Clifford GM, Koulibaly M, Douno K, Kabba I, Haba M, et al. HPV infection in women with and without cervical cancer in Conakry, Guinea. Br J Cancer 2009;101:202-8.  Back to cited text no. 62
[PUBMED]    
63.Begum SA, Rashid MH, Nessa A, Aziz MA, Zakaria SM, Roy JS. Comparative study between Pap smear and visual inspection using acetic acid as a method of cervical cancer screening. Mymensingh Med J 2012;21:145-50.  Back to cited text no. 63
[PUBMED]    
64.Sellors J, Lewis K, Kidula N, Muhombe K, Tsu V, Herdman C. Screening and management of precancerous lesions to prevent cervical cancer in low-resource settings. Asian Pac J Cancer Prev 2003;4:277-80.  Back to cited text no. 64
[PUBMED]    
65.Firnhaber C, Westreich D, Schulze D, Williams S, Siminya M, Michelow P, et al. Highly active antiretroviral therapy and cervical dysplasia in HIV-positive women in South Africa. J Int AIDS Soc 2012;15:17382.  Back to cited text no. 65
[PUBMED]    
66.Adler DH, Kakinami L, Modisenyane T, Tshabangu N, Mohapi L, De Bruyn G, et al. Increased regression and decreased incidence of human papillomavirus-related cervical lesions among HIV-infected women on HAART. AIDS 2012;26:1645-52.  Back to cited text no. 66
[PUBMED]    
67.Bhatla N, Puri K, Kriplani A, Iyer VK, Mathur SR, Mani K, et al. Adjunctive testing for cervical cancer screening in low resource settings. Aust N Z J Obstet Gynaecol 2012;52:133-9.  Back to cited text no. 67
[PUBMED]    
68.Fei HL, Cheng YF, Cheng XD, Chen XD, Ye F, Lu WG, et al. Evaluation of five screening methods for an early detection of cervical cancer and its precancerous lesions in Zhejiang province. Zhonghua Yi Xue Za Zhi 2011;91:309-12.  Back to cited text no. 68
    
69.Kuhn L, Wang C, Tsai WY, Wright TC, Denny L. Efficacy of human papillomavirus-based screen-and-treat for cervical cancer prevention among HIV-infected women. AIDS 2010;24:2553-61.  Back to cited text no. 69
[PUBMED]    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]


This article has been cited by
1 Estimating the costs of HIV clinic integrated versus non-integrated treatment of pre-cancerous cervical lesions and costs of cervical cancer treatment in Kenya
Elisabeth L. Vodicka,Michael H. Chung,Marita R. Zimmermann,Rose J. Kosgei,Fan Lee,Nelly R. Mugo,Timothy C. Okech,Samah R. Sakr,Andy Stergachis,Louis P. Garrison,Joseph B. Babigumira,Bruce A Larson
PLOS ONE. 2019; 14(6): e0217331
[Pubmed] | [DOI]
2 Capabilities, opportunities and motivations for integrating evidence-based strategy for hypertension control into HIV clinics in Southwest Nigeria
Juliet Iwelunmor,Oliver Ezechi,Chisom Obiezu-Umeh,Titilola Gbajabiamila,Adesola Z. Musa,David Oladele,Ifeoma Idigbe,Aigbe Ohihoin,Joyce Gyamfi,Angela Aifah,Babatunde Salako,Olugbenga Ogedegbe,Kwasi Torpey
PLOS ONE. 2019; 14(6): e0217703
[Pubmed] | [DOI]
3 Association between patient-reported HIV status and provider recommendation for screening in an opportunistic cervical Cancer screening setting in Jos, Nigeria
Jonah Musa,Chad J. Achenbach,Charlesnika T. Evans,Neil Jordan,Patrick H. Daru,Lifang Hou,Robert L. Murphy,Isaac F. Adewole,Melissa A. Simon
BMC Health Services Research. 2018; 18(1)
[Pubmed] | [DOI]
4 Implementation science for integration of HIV and non-communicable disease services in sub-Saharan Africa
Christopher G. Kemp,Bryan J. Weiner,Kenneth H. Sherr,Linda E. Kupfer,Peter K. Cherutich,David Wilson,Elvin H. Geng,Judith N. Wasserheit
AIDS. 2018; 32: S93
[Pubmed] | [DOI]
5 Population risk factors for late-stage presentation of cervical cancer in sub-Saharan Africa
Tessa S. Stewart,Jennifer Moodley,Fiona M. Walter
Cancer Epidemiology. 2018; 53: 81
[Pubmed] | [DOI]
6 Integrating cervical cancer screening and preventive treatment with family planning and HIV-related services
Heather L. White,Alejandra Meglioli,Raveena Chowdhury,Olivia Nuccio
International Journal of Gynecology & Obstetrics. 2017; 138: 41
[Pubmed] | [DOI]
7 The Current Status of Research on the Integration of Sexual and Reproductive Health and HIV Services
Charlotte E. Warren,Susannah H. Mayhew,Jonathan Hopkins
Studies in Family Planning. 2017; 48(2): 91
[Pubmed] | [DOI]
8 Non-communicable diseases and HIV care and treatment: models of integrated service delivery
Malia Duffy,Bisola Ojikutu,Soa Andrian,Elaine Sohng,Thomas Minior,Lisa R. Hirschhorn
Tropical Medicine & International Health. 2017;
[Pubmed] | [DOI]
9 Integrating Human Immunodeficiency Virus and Reproductive, Maternal and Child, and Tuberculosis Health Services Within National Health Systems
Dvora Joseph Davey,Landon Myer,Elizabeth Bukusi,Doreen Ramogola-Masire,William Kilembe,Jeffrey D Klausner
Current HIV/AIDS Reports. 2016;
[Pubmed] | [DOI]
10 Cervical Neoplasia in Women Living With HIV at Cervical Cancer Screening Clinics in Mutare, Eastern Zimbabwe
Auxilia Chideme Munodawafa
Journal of Gynecology & Neonatal Biology. 2016; 2(2): 1
[Pubmed] | [DOI]
11 Integration of HIV and cervical cancer screening perceptions of healthcare providers and policy makers in Uganda
Edward Kumakech,Sören Andersson,Henry Wabinga,Vanja Berggren
BMC Public Health. 2014; 14(1): 810
[Pubmed] | [DOI]
12 High-risk human papilloma virus and cervical abnormalities in HIV-infected women with normal cervical cytology
Jonah Musa,Chad Achenbach,Babafemi Taiwo,Baiba Berzins,Olugbenga Silas,Patrick H Daru,Oche Agbaji,Godwin Imade,Atiene S Sagay,John A Idoko,Phyllis J Kanki,Robert L Murphy
Infectious Agents and Cancer. 2014; 9(1): 36
[Pubmed] | [DOI]



 

Top
  
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
   Acknowledgments
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed3896    
    Printed107    
    Emailed0    
    PDF Downloaded218    
    Comments [Add]    
    Cited by others 12    

Recommend this journal