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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
J Infect Dis. Author manuscript; available in PMC Feb 1, 2010.
Published in final edited form as:
PMCID: PMC2814215

Human Papillomavirus Infection and Cervical Cytology in HIV-Infected and HIV-Uninfected Rwandan Women



Data on human papillomavirus (HPV) prevalence are essential for developing cost-effective cervical cancer prevention programs.


In 2005, 710 human immunodeficiency virus (HIV)–positive and 226 HIV-negative Rwandan women enrolled in an observational prospective cohort study. Sociodemographic data, CD4+ cell counts, and cervical specimens were obtained. Cervicovaginal lavage specimens were collected from each woman and tested for >40 HPV types by a polymerase chain reaction assay; HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, and 68 were considered primary carcinogenic HPV types.


The prevalence of HPV was higher in HIV-positive women than in HIV-negative women in all age groups. Among HIV-infected women, 69% were positive for ≥1 HPV type, 46% for a carcinogenic HPV type, and 10% for HPV-16. HPV prevalence peaked at 75% in the HIV-positive women aged 25–34 years and then declined with age to 37.5% in those ≥55 years old (Ptrend < .001). A significant trend of higher prevalence of HPV and carcinogenic HPV with lower CD4+ cell counts and increasing cytologic severity was seen among HIV-positive women.


We found a higher prevalence of HPV infection in HIV-positive than in HIV-negative Rwandan women, and the prevalence of HPV and carcinogenic HPV infection decreased with age.

Infections by 15–20 cancer-associated (“carcinogenic”) human papillomavirus (HPV) types cause virtually all cervical cancers and their immediate precursor lesions [1]. HPV-16 and HPV-18 are the most important HPV types, causing ~70% of cancers and 50%– 60% of cervical precancerous lesions. Recently developed prophylactic HPV vaccines targeting HPV-16 and HPV-18 have demonstrated >90% efficacy against these types in unexposed women; the next generation of vaccines may target a broader array of HPV types [26]. Because the vaccine does not provide complete protection and is not currently affordable in many regions, and because a substantial number of women have already been exposed to HPV, screening for HPV infection and/or cervical neoplasia continues to be necessary to reduce the risk of cervical cancer.

Worldwide, >80% of cervical cancer incidence and mortality occur in resource-limited regions, where women are medically underserved and have little or no access to preventive health services [7]. Data from developing countries on the overall prevalence of HPV and carcinogenic HPV infection, age-specific prevalence, and the most important HPV types are thus needed to inform rational implementation of HPV vaccination and screening strategies in these areas. Knowledge of the median age of sexual debut in the population and of the peak of age-specific prevalence is useful for the timing of HPV vaccination, which is highly effective in preventing infection but does not treat preexisting infections [26, 810]. The prevalence of HPV infection among older women will help determine which screening method should be considered, because excessive prevalence of HPV infection will render HPV testing too nonspecific for cervical precancer and cancer detection to be clinically useful. Africa, along with Latin America, bears the greatest burden of cervical cancer globally [11]. Regional and, preferably, local data on HPV infection are thus needed to guide these decisions in politically, religiously, and economically diverse continents.

Most data on HPV infection prevalence among human immunodeficiency virus (HIV)–infected women from Africa come from a few countries, including Uganda, Senegal, and South Africa. It is unclear how representative these sites are in relation to regional HPV infection patterns in other African countries. The prevalence of HPV infection can vary significantly between adjacent regions with similar ethnic and cultural identities, owing to recent social and political upheaval, as observed in North and South Vietnam [12]. In 1994, Rwanda was dramatically affected by rape, violence, and social upheaval, and cytology-based cervical cancer prevention screening is not currently available for most Rwandan women. There are few data on HIV infection, HPV infection, and cervical cancer in Rwanda, owing to limited research and public health infrastructure, including the loss of many expert health care workers during the 1994 genocide. During 1991–1993, cervical cancer was the most common malignancy among Rwandan women, accounting for 22% of all cancer cases among women in the Butare prefecture [13]. Cervical cancer precursors were also common, especially among HIV-infected women, with squamous intraepithelial lesions (SILs) of the cervix found in 24% and high-grade SILs (HSILs) in 10% of HIV-infected pregnant women in a 1992–1993 Rwandan survey [14]. A more recent retrospective study conducted in 2005 found that cervical cancer represented 27% of diagnosed cancer cases among women [15].

We report here an epidemiologic study performed to characterize the spectrum of HPV types in HIV-positive and HIV-negative Rwandan women and to identify risk factors for HPV infection among these women. These data are essential for developing cost-effective cervical cancer prevention programs in Rwanda.


Participants and specimens

The Rwanda Women’s Interassociation Study and Assessment (RWISA) is an observational prospective cohort study of 710 HIV-infected and 226 HIV-uninfected Rwandan women enrolled between 15 May and 15 November 2005. Participants were recruited through grassroots women’s organizations and clinical care sites for HIV-infected patients. Inclusion criteria were age of ≥25 years at study entry, willingness to give informed consent, presence in Rwanda during 1994, and no history of receiving antiretroviral treatment except single-dose nevirapine to prevent mother-to-child transmission of HIV. Included in this analysis are all RWISA participants for whom both cytologic and HPV typing findings were available. Informed consent was obtained with protocols approved by the Rwandan National Ethics Committee and the Institutional Review Board of Montefiore Medical Center. At study entry, participants provided data on sociodemographic characteristics, sexual behaviors, medical history, psychosocial history, experiences of trauma during the 1994 Rwandan genocide, and symptoms of depression and posttraumatic stress. A physical examination was performed, and blood specimens were obtained for determination of CD4+ cell count and full blood count and performance of other laboratory tests. In a balanced factorial study design, 50% of the participants had experienced rape during the 1994 genocide, and 75% were HIV-1 infected.

Participants underwent physical and pelvic examinations. To minimize contamination of gynecologic specimens by blood, exfoliated cervical cells (used for HPV DNA testing) were obtained by cervicovaginal lavage (CVL) before collection of a cervical cytologic specimen. Briefly, 10 mL of 0.9% saline was sprayed against the cervical os and the exocervix. The CVL specimen was aspirated from the posterior vaginal fornix and transported to the laboratory within 2 h. The specimen was mixed gently by vortexing to distribute cells, divided into 1-mL aliquots, and stored at −70°C until it was used for HPV DNA testing. After collection of CVL specimens, cervical smear samples were obtained for cytologic analysis from each participant, using a wooden Ayres spatula and a cytologic brush.

Clinical laboratory data

CD4+ cell counts were measured at the National Reference Laboratory of Rwanda by a FACS-Count system (Becton Dickinson). Full blood counts, liver function values, and serum lipoprotein levels were determined by standard methods at the clinical laboratory of King Faisal Hospital in Kigali.

HPV testing

HPV testing was performed on CVL specimens obtained at the enrollment visit. In brief, 100 μL of each CVL specimen was mixed (ratio, 1:1) with a 2× solution of K buffer (400 g/mL proteinase K, 2 mmol/L ethylenediaminetetraacetic acid, 2% laureth-12, and 100 mmol/L Tris [pH 8.5]) and incubated at 55°C for 2 h, followed by another period of incubation at 95°C for 10 min. After the CVL specimens were digested with proteinase K, 10 μL of each cell digest was obtained to detect HPV DNA, using the L1 MY09/MY11 modified polymerase chain reaction (PCR) system with AmpliTaq Gold polymerase, as described elsewhere [16]. Amplification products were probed for the presence of any HPV DNA by Southern blot analysis with a radiolabeled generic probe mixture and subsequently typed by dot blot hybridization for HPV types 6, 11, 13, 16, 18, 26, 31–35, 39, 40, 42, 45, 51–59, 61, 62, 64, 66–74, 81–85, 89, and 97.

In this analysis, HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, and 68 were considered the primary carcinogenic HPV types [16]. Women were also assigned to the following HPV infection risk groups, established a priori, that were based on cervical cancer risk (HPV-16 had the most severe risk, followed by HPV-18, carcinogenic HPV, noncarcinogenic HPV, and PCR-confirmed HPV negativity): (1) positive for HPV-16, (2) negative for HPV-16 and positive for HPV-18, (3) positive for other carcinogenic HPV types but not for HPV-16 and HPV-18, (4) positive for noncarcinogenic HPV types and negative for all carcinogenic HPV types, and (5) HPV negative by PCR.

Cytologic analysis

Cytology smear samples were examined by cytopathologists in the United States at Evanston Hospital in Illinois or Montefiore Medical Center in New York and were categorized using the Bethesda system for cytologic interpretation [17].

Data analysis

The exposure variables of primary interest for the HPV analyses were HIV infection, CD4+ cell count, and, for cytologic outcomes, the genotype of HPV infection. Interpretations of cytologic findings with a severity of HSIL or greater (hereafter, “HSIL+”) also included the following categories: atypical glandular cells; atypical squamous cells of undetermined significance (ASCUS), cannot exclude HSIL; atypical glandular cells, favor neoplastic; adenocarcinoma in situ; adenocarcinoma; and squamous carcinoma. In some analyses, all non-normal cytologic findings, defined as those with a severity of ASCUS or greater (hereafter, “≥ASCUS”), were categorized together and compared with normal findings (i.e., findings negative for any intraepithelial lesion or malignancy [NILM]). Secondary exposure variables included age, body mass index (BMI, calculated as the weight in kilograms divided by the height in meters squared), number of consensual and nonconsensual sexual partners, age at first consensual or nonconsensual intercourse, exposure to genocidal rape, number of cohabitants, average number of meals per week with meat, and number of previous pregnancies. Underweight was defined as a BMI of <18.5; normal weight, as 18.5–24.9; overweight, as 25.0 –29.9; and obesity, as ≥30 [18].

Descriptive statistics, including medians, interquartile ranges, numbers, and percentages, were summarized and used to compare outcomes and characteristics of the overall cohort after stratification by HIV infection status and other characteristics. Exact tests compared categorical variables by exposure groups, and t tests or Wilcoxon rank tests were used to compare continuous variables. Standard contingency table methods, calculated by means of exact tests, were used to assess possible univariate associations of categorical variables with HPV. Confidence intervals (CIs) for proportions were calculated using exact methods. Odds ratios (ORs) and 95% CIs adjusted for parameters that were identified during preliminary data analysis as being relevant were determined using multivariate logistic regression. Stepwise forward selection models with SAS default entry and removal criteria were fit to build the final models, as shown in table 1, with selection based on “any HPV” as the outcome. Data were analyzed with SAS software (version 9.3; SAS), and differences were considered statistically significant at P < .05.

Table 1
Risk factors associated with prevalent human papillomavirus (HPV) detection among human immunodeficiency virus–positive women in multivariate logistic models that include all listed variables.


Cytologic and HPV data were available for 647 (91%) of 710 HIV-positive women and 188 (83%) of 226 HIV-negative women (table 2). Missing cytologic data was the most common reason for exclusion; 36 HIV-uninfected participants and 60 HIV-infected participants lacked cytologic data, whereas HPV data were missing for 2 HIV-uninfected participants and 3 HIV-infected participants (P = .9). HIV-positive women were younger (P < .001), had first experienced sex at an earlier age (P = .05), and had had more lifetime sexual partners (P < .001) and fewer pregnancies (P < .001) than HIV-negative women. There were no significant differences in BMI stratified by HIV serostatus (P = .9).

Table 2
Sociodemographic and clinical characteristics of human immunodeficiency virus (HIV)–negative and HIV-positive Rwandan women.

Because of the significant age differences between the 2 study groups, we examined the age-specific prevalence for any HPV type and any carcinogenic HPV type (figure 1). The prevalence of HPV infection was higher among HIV-positive women than among HIV-negative women for all age groups (25–34 years, 75% vs. 29%; 35– 44 years, 64% vs. 7%; 45–54 years, 57% vs. 13% [P < .001 for all]; and ≥55 years, 38% vs. 0% [P = .02]); similar differences between HIV-positive and HIV-negative women were observed for carcinogenic HPV, except the difference in the ≥55-year age group was not statistically significant. Prevalences of HPV and carcinogenic HPV infection among HIV-positive women were highest in the 25–34-year age group (75% and 50%, respectively) and decreased with age (Ptrend < .001). Similar patterns were observed for HIV-negative women. Because of the small numbers of HIV-negative women, the low prevalence of HPV infection in this group, and the differences in the age distribution between HIV-negative and HIV-positive women, we restricted further analyses to HIV-positive women only.

Figure 1
Prevalence of infection with any human papillomavirus (HPV) type (A) and any carcinogenic HPV type (B), by age group and human immunodeficiency virus (HIV) infection status. A, Prevalence of HPV infection differed significantly according to age among ...

Differences in the prevalence of HPV infection, stratified by CD4+ cell count, among HIV-positive women are shown in table 3. Overall, 69% of HIV-infected women were positive for ≥1 type of HPV, 46% were positive for a carcinogenic HPV type, and 10% were positive for HPV-16. Prevalence of infection with carcinogenic HPV, excluding types 16 and 18, was significantly higher with lower CD4+ cell counts (Ptrend = .004), whereas neither HPV-16 nor HPV-18 was significantly associated with CD4+ cell count. The proportion of women infected by multiple (≥2) HPV genotypes was significantly higher with lower CD4+ cell counts, with twice the proportion of multigenotype HPV infections among women with a CD4+ cell count of <200 cells/μL, compared with women with a CD4+ cell count of ≥350 cells/μL (48% vs. 24%). Exposure to genocidal rape was not significantly associated with the prevalence of HPV infection (67% among women with and 71% among women without exposure to rape) or the prevalence of carcinogenic HPV infection (45% and 46%, respectively). Similarly, the prevalence of HPV infection among HIV-negative women exposed to rape (18%) was not statistically significant from the prevalence among those who were not exposed to rape (11%). We also evaluated the prevalence of HPV infection, grouped by phylogenetic species, according to CD4+ cell status among HIV-positive women. Higher prevalence with worse immune function (i.e., lower CD4+ cell counts) was seen with all HPV species although the effect was greatest for those infected with α-11 and α-5 types and least for α-9 types, which includes HPV-16 (table 3).

Table 3
Prevalence of human papillomavirus (HPV), overall and by CD4+ cell count, among human immunodeficiency virus–positive women.

Increasing severity of cervical cytologic interpretations was associated with higher prevalence of HPV and carcinogenic HPV infection among HIV-positive women (Ptrend < .001 for both) (table 4). Among HIV-positive women, the prevalence of HPV and carcinogenic HPV infection was 60% and 33%, respectively, for those with NILM, and 94% and 80%, respectively, for those with HSIL+. HPV-16 prevalence increased from 6% in women with NILM to 23% among women with HSIL+(Ptrend < .001). The prevalence of carcinogenic HPV infection, excluding HPV-16 and HPV-18, increased from 23% among women with NILM to 51% among women with HSIL (Ptrend < .001). The prevalence of HPV-18 (without HPV-16) among women with HSIL+ (6%) was less than that among women with either ASCUS (9%) or low-grade SIL (LSIL; 9%) (Ptrend = .05). The prevalence of HPV infection, grouped by phylogenetic species, was examined according to the presence of equivocal or abnormal cytologic findings (ASCUS, LSIL, or HSIL+ vs. normal cytologic findings). HPV infections with α-9 and α-5 HPV types were most often associated with abnormal cytologic findings, with an overall ratio of 2.4:1 for women with ≥ASCUS versus those with normal findings (P < .001).

Table 4
Prevalence of human papillomavirus (HPV), overall and by cytologic finding, among human immunodeficiency virus–positive women.

The combined associations of abnormal cytologic findings and immunosuppression with the prevalence of HPV infection were assessed among HIV–positive women (table 5). Almost all women (91%) with a CD4+ cell count of <200 cells/μL and abnormal cytologic findings were positive for HPV, compared with only approximately half of women (49%) with a CD4+ cell count of >350 cells/μL and normal cytologic findings. Similar trends were seen for infection with carcinogenic HPV. Infection with HPV-16 was much more likely among women with abnormal cytologic findings (5%– 8% for women with NILM vs. 16%–18% for those with ≥ASCUS; P < .05 for all) but varied minimally across CD4+ cell count strata.

Table 5
Prevalence of any human papillomavirus (HPV), any carcinogenic HPV, and HPV-16, by CD4+ cell count and cytologic finding, among human immunodeficiency virus–positive women.

In the final stepwise multivariate logistic regression model for prevalence of any HPV infection among HIV-positive women (table 1), factors independently associated with HPV positivity were CD4+ cell counts of <200 cells/μL (OR, 4.0 [95% CI, 2.4 –6.6]) or 200 –350 cells/μL (OR, 1.8 [95% CI, 1.1–2.7]), compared with counts of >350 cells/μL; eating meat 1–2 times a week (OR, 1.7 [95% CI, 1.1–2.7]) or ≥3 times a week (OR, 2.8 [95% CI, 1.5–5.4]), compared with eating no meat; and self-report of 1–2 gynecologic infections in the past (OR, 2.1 [95% CI, 1.4 –3.2]), compared with no prior gynecologic infection. A lower risk of HPV infection was independently associated with obesity (OR, 0.3 [95% CI, 0.1– 0.9]), compared with no exposure to rape during the 1994 genocide (OR, 0.6 [95% CI, 0.4 –1.0]). Similar findings were noted for carcinogenic HPV (table 1).


HIV-seropositive Rwandan women in our study had high prevalences of infection with HPV (69%), carcinogenic HPV (46%), and multiple HPV types (35%), which in turn were associated with higher risk of abnormal cervical cytologic findings. Our findings are consistent with work reported elsewhere, which found high rates of HPV infection, including multiple HPV types among HIV-positive women [19]. In 1 study of 236 women from the rural northwestern part of Zimbabwe, the prevalence of HPV infection among HIV-positive women was 2 times the prevalence among HIV-negative women (54% vs. 27%) [20]. Clifford et al. [19] found that 32.8% of HIV-positive women who were positive for HPV were infected with multiple HPV types. In a group of 208 HIV-infected women who were studied in Brazil, 98% were positive for HPV and 79% were positive for multiple HPV types, with an average of 3 HPV types detected per woman [21]. Of the types detected, 59% were carcinogenic. Neither of these studies included an HIV-negative comparison group.

Among our participants with HSIL, only 23% harbored HPV-16, whereas 57% were positive for multiple HPV types. Although the number of participants with HSIL was small, our findings are consistent with those of work reported elsewhere, including the recent meta-analyses by Clifford and colleagues, who found high rates of infections involving multiple HPV types among HIV-positive women with HSIL (41% in the HIV-positive group versus 7% in populations with unknown HIV serostatus) as well as an underrepresentation of HPV-16 among HIV-positive women with HSIL (32% among HIV-positive women vs. 45% in the general population) [19, 22]. In another study of Zimbabwean women, 523 infections were identified in 162 women with HSIL, with fewer women having single infections (52 [32%] of 162) than multiple infections (110 [68%] of 162) [23].

Although it may seem counterintuitive that genocidal rape was negatively associated with HPV infection, among this socially conservative group our data indicate that many women who experienced genocidal rape ~10 years before the study were subsequently abstinent or had very few partners, thus limited their exposure to new HPV infections. This is consistent with other findings suggesting that women change their behaviors after sexual violence [24].

Our finding that greater meat consumption was associated with higher prevalence of HPV infection may reflect meat as a marker for affluence, which in turn may be associated with more partners among the male partners of RWISA participants. In Rwanda and elsewhere in Africa, higher income has been associated with increased risk for HIV infection [25]. Researchers have postulated that wealthier men may be more mobile, more likely to have multiple partners, and more likely to engage in sex with nonregular partners [25]. All of these male behaviors can increase the risk of HPV exposure in their usual partners. However, this is the first report of an association of meat consumption with HPV positivity and could be a chance finding.

Limitations of our study of HPV infection among Rwandan women include the small number of HIV-negative participants and the age difference between the HIV-positive and HIV-negative women, which may influence both HPV infection prevalence and cytologic findings. In addition, the use of CVL specimens for HPV testing may have overrepresented noncarcinogenic HPV types with a tropism for the vagina, such as the α–3/α–15 phylogenetic species [26].

Our report provides initial data on Rwandan women, a poorly studied population that remains at elevated risk of morbidity and mortality related to cervical cancer and was previously unscreened for cervical abnormalities and HPV infection. Among HIV-positive women, we found a high prevalence of HPV and carcinogenic HPV infection that decreased with age. HPV types other than HPV-16 had a particularly higher prevalence among immunosuppressed women. In the past decade, significant strides have been made in the prevention, detection, and treatment of cervical cancer. With ongoing research and commitment from global policy makers, such services can be provided to these highest-risk populations. These data will help guide cervical cancer prevention strategies in Rwanda.


National Institute of Allergy and Infectious Diseases (NIAID) and National Cancer Institute (NCI) (supplements to Bronx/Manhattan Women’s Interagency HIV Study, funded by NIAID [grant UO1-AI-35004]); Center for AIDS Research, Albert Einstein College of Medicine and Montefiore Medical Center (funded by National Institutes of Health [grant NIH AI-51519] and by National Institute of Diabetes and Digestive and Kidney Disease [grant DK54615]); NCI intramural research program.


Potential conflicts of interest: none reported.

Presented in part: 37th annual meeting of the Society of Gynecologic Oncology, Palm Springs, California, 22–26 March 2006 (poster and oral presentation formats).


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