RESEARCH ARTI CLE Open Access

HIV associated high-risk HPV infection among

Nigerian women
Sally N Akarolo-Anthony
1,2*
, Maryam Al-Mujtaba
2
, Ayotunde O Famooto
2
, Eileen O Dareng
2
, Olayinka B Olaniyan
3
,
Richard Offiong
4
, Cosette M Wheeler
5
and Clement A Adebamowo
1,2,6
Abstract
Background: In developed countries, the incidence of cervical cancer has remained stable in HIV+ women but the
prevalence and multiplicity of high-risk HPV (hrHPV) infection, a necessary cause of cervical cancer, appears different
comparing HIV+ to HIV- women. Little is known about HIV and HPV co-infection in Africa.
Methods: We enrolled women presenting at our cervical cancer screening program in Abuja, Nigeria between April
and August 2012, and collected information on demographic characteristics, risk factors of HPV infection and
samples of exfoliated cervical cells. We used Roche Linear Array HPV Genotyping Test to characterize prevalent
HPV and logistic regression models to estimate the association between HIV and the risk of hrHPV infection.
Results: There were 278 participants, 54% (151) were HIV+, 40% (111) were HIV-, and 6% (16) had unknown HIV
status. Of these, data from 149 HIV+ and 108 HIV- women were available for analysis. The mean ages (SD) were
37.6 (7.7) years for HIV+ and 36.6 (7.9) years for HIV- women (p-value = 0.34). Among the HIV+ women, HPV35
(8.7%) and HPV56 (7.4%) were the most prevalent hrHPV, while HPV52 and HPV68 (2.8%, each) were the most preva-
lent hrHPV types among HIV- women. The multivariate prevalence ratio for any hrHPV and multiple hrHPV infections
were 4.18 (95% CI 2.05 8.49, p-value <0.0001) and 6.6 (95% CI 1.49 29.64, p-value 0.01) respectively, comparing
HIV + to HIV- women, adjusted for age, and educational level.
Conclusions: HIV infection was associated with increased risk of any HPV, hrHPV and multiple HPV infections.
Oncogenic HPV types 35, 52, 56 and 68 may be more important risk factors for cervical pre-cancer and cancer
among women in Africa. Polyvalent hrHPV vaccines meant for African populations should protect against other
hrHPV types, in addition to 16 and 18.
Keywords: HIV, HPV, Nigeria
Background
Human papillomavirus (HPV) is the most common sexu-
ally transmitted infection and at least 50% of sexually ac-
tive people will get HPV at some time in their lives[1,2].
More than 100 HPV genotypes have been identified
based on the sequence of their L1 genes [1,3]. HPV are
classified into high-risk, probable high-risk and low-risk
types, based on HPV-type-specific odds ratios and HPV
prevalence among groups of women with cervical cancer
and their controls [4]. HPV types 16, 18, 31, 33, 35, 39,
45, 51, 52, 56, 58, 59, 68, 73, and 82 are considered high-
risk HPV (hrHPV) [4,5]. In addition to already estab-
lished types, the International Agency for Cancer Re-
search (IARC) recently classified HPV39, 59, 51 and 56
as carcinogenic while HPV68, 26, 30, 34, 53, 66, 67, 69,
70, 73, 82 and 85 were classified as possibly carcinogenic
[6,7], but this classification has been criticized for lack of
supporting epidemiological data [8]. The classification of
HPV types according to their oncogenic potential is an
ongoing process and is dependent on availability of data
from different parts of the world.
Persistent hrHPV infection is recognized as a necessary
but not sufficient cause for Cervical Intraepithelial Neo-
plasm (CIN) grades 2/3 and cervical cancer [9]. Molecular
genetic studies of hrHPV from most parts of the world
* Correspondence: [email protected]
1
Department of Nutrition, Harvard School of Public Health, 677 Huntington
Avenue, Boston, MA 02115, USA
2
Office of Strategic Information and Research Department, Institute of
Human Virology Nigeria, 252 Herbert Macaulay Way, Abuja, Nigeria
Full list of author information is available at the end of the article
2013 Akarolo-Anthony et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the
Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
Akarolo-Anthony et al. BMC Infectious Diseases 2013, 13:521
http://www.biomedcentral.com/1471-2334/13/521
suggest that types 16 and 18 are the most prevalent types
associated with CIN2 + [10,11]. This has been supported
by several meta-analyses [8,12]. However these studies
contained few high quality data from Africa and their re-
sults are liable to be biased by the availability and source of
data. In the latest meta-analysis for example, inclusion of
data from Eastern Asia inflated the prevalence of HPV58
suggesting that similar situation may occur as more data
accrue from other parts of the world [9,10,13-17].
Although the limited data available suggests that the
incidence and mortality from cervical cancer in Africa
has not changed significantly in the last few decades des-
pite the HIV/AIDS epidemic [18-21], HIV infection may
result in different HPV distributions in cancer, within
sub-Saharan Africa [22]. Several studies show that HIV+
women are more likely to be infected with non-16 and
non-18 hrHPV types including HPV51, 53 and 56 as
well as with multiple infections [23,24]. Studies done in
Africa to date suggest that the most prevalent hrHPV
types are HPV16, 52, 53 and 58 in HIV+ women, com-
pared to HPV52 and 51 in HIV- women [16,25,26].
However, these studies were based on East African pop-
ulations, in Uganda, Rwanda and Zambia. There is
scarce data about the prevalent hrHPV among HIV+
women in West African populations. One study found
the most prevalent types of hrHPV among women in
Abidjan, Cote dIvoire to be HPV16 and 35, regardless of
HIV status [27]. Given that cervical cancer incidence is
~50% higher in East compared to West Africa [28,29] we
hypothesized that the prevalence, types and multiplicity of
Table 1 Characteristics of the study population, by HIV status
Characteristics HIV positive (n = 149) HIV negative (n = 108) HIV positive (n = 149) HIV negative (n = 108) p-value
Mean (SD) Mean (SD) N (%) N (%)
Age
#
36.6 (7.9) 37.6 (7.7) 0.34
Age categories
#
0.30
- 30 35 (23.7) 23 (21.3)
- 31 36 44 (29.7) 22 (20.4)
- 37 44 47 (31.7) 44 (40.7)
- 45 22 (14.9) 19 (17.6)
Age at sexual initiaton
#
20.8 (4.4) 19.2 (3.9) 0.004
Age at sexual initiation
#
0.005
- < 18 41 (28.7) 21 (19.4)
- 18 21 68 (47.5) 50 (46.3)
- 22 - 25 26 (18.2) 16 (14.8)
- > 25 8 (5.6) 21 (19.5)
Total sex partners 3.3 (3.2) 3.9 (5.5) 0.34
Total sex partners 0.54
- 1 35 (23.7) 34 (31.5)
- 2 3 68 (46.0) 40 (37.0)
- 4 5 27 (18.2) 18 (16.7)
- 5+ 18 (8.1) 15 (13.8)
Education 0.002
- 6 years 28 (18.8) 7 (6.5)
- Secondary 104 (69.8) 76 (70.4)
- Tertiary 17 (11.4) 25 (23.1)
Marital Status <0.001
- Married, % 76 (51.0) 82 (75.9)
- Not married, % 73 (49.0) 26 (24.1)
Condom use* 0.26
- Yes 3 (2.0) 0 (0)
- No 146 (98.0) 108 (100)
#
Age in years.
*Consistent condom use in the past 2 years.
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hrHPV infections might differ between East and West
African populations and are likely to be associated with
the rates of cervical cancer in these populations.
Methods
Study population
Between April and August 2012, we enrolled 278 women
from 3 cervical cancer screening clinics at National Hos-
pital Abuja and University of Abuja Teaching Hospital,
Nigeria. All the study participants were 18 years or older,
had prior vaginal sexual intercourse, not pregnant and
had an intact uterus. Interviewer administered question-
naires were used to collect data on socio-demographic
characteristics, HIV status, sexual and reproductive
history. Participants HIV status were confirmed from
their medical records. Trained nurses performed pelvic
examinations on all the study participants. Samples of
exfoliated cervical cells were obtained from the cervical os
using Ayres spatula and stored at 80C, until processing
for HPVgenotyping.
HPV detection by genotyping
HPV DNA genotyping was done using linear array to
HPV genotyping test (Roche Diagnostics), a qualitative
in vitro test which utilizes amplification of target DNA by
the Polymerase Chain Reaction (PCR) and nucleic acid
hybridization and detects 37 high- and low-risk HPV ge-
notypes [30]. The Linear Array HPV genotyping test has
been validated and offers reliable and sensitive approach
for detecting HPV DNA in cervical specimens, using stan-
dardized quality-controlled reagents [31-35].
Data management
Data was managed using REDCap electronic data cap-
ture tools, hosted at the Institute of Human Virology,
Nigeria (IHVN) [36,37].
Statistical analysis
A total of 278 participants were enrolled in this study.
We excluded 16 persons whose HIV status were not
confirmed and 5 persons who had missing data on HPV
genotype or several demographic variables. Descriptive
analyses were performed to characterize the sampled
population. t-tests were used to assess differences in the
distribution of continuous variables between groups,
while
2
and Fishers exact tests were used for categorical
variables. Multivariate logistic regression models were
conducted to examine the association between HIV sta-
tus and risk of hrHPV infections. All analyses were per-
formed using SAS 9.3 for UNIX statistical software (SAS
Institute, Cary, NC, USA).
Table 2 Prevalence of specific high-risk HPV types by HIV
status, among Nigerian women
HrHPV
type
HIV positive [n = 149] HIV negative [n = 108] p-value
N (%) N (%)
16 5 (3.4) 1 (0.9) 0.41
18 5 (3.4) 2 (1.9) 0.70
31 3 (2.0) 1 (0.9) 0.64
33 6 (4.0) 0 (0.0) 0.04
35 13 (8.7) 0 (0.0) <0.001
39 4 (2.7) 2 (1.9) 1.0
45 7 (4.7) 2 (1.9) 0.31
51 4 (2.7) 0 (0.0) 0.14
52 3 (2.0) 3 (2.8) 0.69
56 11 (7.4) 1 (0.9) 0.01
58 10 (6.7) 0 (0.0) 0.006
59 8 (5.4) 1 (0.9) 0.08
68 5 (3.4) 3 (2.8) 1.0
Figure 1 Frequency of high risk HPV types among Nigerian women, by HIV status.
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Ethics
The study was conducted according to the Nigerian
National Code for Health Research Ethics and the Dec-
laration of Helsinki. Ethical approval to conduct this
study was obtained from the IHVN health research eth-
ics committee. Informed consent was obtained from all
participants before enrollment in the study.
Results
We analyzed data on 257 women, of whom 58% (149/
257) were HIV+ and 42% (108/257) were HIV-. The
mean age and standard deviation (SD) of the partici-
pants was 36.6 (7.9) years for the HIV+ and 37.6 (7.7)
years for the HIV- women. Half (51%) of the HIV+
women were married, compared to 76% of the HIV-
women who were married. The mean age at sexual
initiation was 20.8 (4.4) years for the HIV+ women, com-
pared to 19.2 (3.9) for the HIV- women, p-value = 0.004.
HIV+ and HIV- women did not differ by total number
of sexual partners or consistent condom use. Table 1
describes the demographic characteristics of the study
participants by HIVstatus.
The prevalence of hrHPV infection was 25% (64/257).
Among the HIV+ women, 36% (53/149) had hrHPV infec-
tions, while 10% (11/108) of the HIV- women had hrHPV
infections (p = <0.001). Thirteen specific hrHPV types were
detected among the HIV+ women and 9 hrHPV types
among the HIV- women. HPV33, 35, 51 and 58 were de-
tected only among the HIV+ women. The most prevalent
hrHPV type in the study population was HPV35; it was de-
tected exclusively in HIV+ women, where it accounted for
24.5% (13/53) of the hrHPV infections. HPV33, 51 and 58
were also detected only in the HIV+ women. The preva-
lence of HPV types 35, 56 and 58 were significantly
different among HIV+ compared with HIV- women
(Table 2). Figure 1 shows the specific hrHPV types among
the women, by HIVstatus
We found single hrHPV infections were more common
66% (42/64), compared to multiple hrHPV infections 34%
(22/64) in the overall study population (p = <0.001).
Among the HIV+women, 14% (21/149) had multiple
hrHPV infections while 2% (2/108) of the HIV- women
had multiple hrHPV infections (p = <0.001). Of the 21 HIV
+ women infected with multiple hrHPVgenotypes, 15 were
infected with two, 5 were infected with three and 1 was in-
fected with six hrHPV types. All the HIV+ women infected
with 2 hrHPV types had HPV35 and another type.
The age adjusted prevalence ratio (PR) of any instance
of single hrHPV infection and any instance of multiple
hrHPV infection comparing HIV+ women to HIV-
women were 4.71 (95% CI 2.34 9.46, p = <0.001) and
8.68 (95% CI 1.99 37.96, p = <0.004) respectively. The
multivariate PR of any hrHPV and multiple hrHPV infec-
tion adjusted for age and education were 4.18 (2.06 - 8.49
p = <0.001) and 6.66 (1.50 - 29.64 p = 0.01) respectively.
Education accounted for most of the variation in these
multivariate models (Table 3).
Discussion and conclusion
Our study shows that the prevalence of hrHPV infection
was significantly higher among HIV+ women, compared
to HIV- women and HIV+ women were more likely to
have multiple hrHPV infections. In decreasing order,
HPV35, 56, 58, 59 and 45 were the most prevalent types
of hrHPV infection found among those who were HIV+
while HPV68, 52, 39, 45 and 18 were the most prevalent
types of hrHPV infection among those who were HIV-,
in our study participants.
Table 3 Prevalence ratios and 95% confidence intervals of high-risk HPV infections, among Nigerian women
Single high risk HPV Multiple high risk HPV
PR (95% CI) p-value PR (95% CI) p-value
Model 1 HIV (Ref = HIV negative) 4.18 (2.06 - 8.49) <0.001 6.66 (1.50 - 29.64) 0.01
Age 0.94 (0.90 - 0.98) 0.001 0.95 (0.89 - 1.01) 0.10
Education 0.58 (0.32 - 1.04) 0.06 0.29 (0.12 - 0.70) 0.006
Model 2 HIV (Ref = HIV negative) 4.76 (2.28 - 9.93) <0.001 7.97 (1.80 - 35.29) 0.006
Age 0.93 (0.89 - 0.97) 0.001 0.95 (0.89 - 1.01) 0.08
No. of sexual partners 0.91 (0.65 - 1.28) 0.58 0.80 (0.48 - 1.34) 0.40
Age at sexual initiation 0.94 (0.66 - 1.35) 0.74 0.71 (0.40 - 1.26) 0.23
Model 3 HIV (Ref = HIV negative) 4.38 (2.06 - 9.30) 0.001 5.93 (1.29 - 27.14) 0.02
Age 0.93 (0.89 - 0.97) 0.001 0.95 (0.89 - 1.01) 0.11
Education 0.64 (0.34 - 1.21) 0.17 0.31 (0.12 - 0.81) 0.02
Marital status 1.03 (0.53 - 2.01) 0.93 1.82 (0.68 - 4.87) 0.23
No. of sexual partners 0.93 (0.65 - 1.32) 0.68 0.78 (0.45 - 1.33) 0.36
Age at sexual initiation 1.00 (0.69 - 1.45) 0.99 0.91 (0.50 - 1.64) 0.74
Akarolo-Anthony et al. BMC Infectious Diseases 2013, 13:521 Page 4 of 6
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Our results are consistent with the findings from other
studies that showed women with HIV infection were
more likely to be infected with non-16 and non-18
hrHPV types [24,38,39]. The most prevalent types of
hrHPV found in this study differ from those in other
populations. Among 208 HIV+ non-pregnant women in
So Paulo, Brazil and 229 HIV+ non-pregnant women in
New York, US, the most common types of hrHPV were
51, 18, 16 and 56, 53, 16, 58 respectively [23,24]. Among
HIV+ pregnant women in Thailand, the most common
hrHPV types were 39, 52, 53 and 16 [39]. In Africa, a
study among HIV+ and HIV- women in Kampala,
Uganda found the most prevalent types of hrHPV to be
52, 16 and 58, and these where similar to findings in
Nairobi, Kenya [25,40]. In Kigali, Rwanda, the most
prevalent hrHPV type among HIV+ women was also
HPV52, followed by HPV51 and 58 [16].
Our findings were similar to the results from other
studies in Nigeria. Cage et al. found non-16 and non-18
HPV were the most prevalent hrHPV types [41]; Okolo
et al. found HPV35 was as prevalent as HPV16; Musa
et al. found the prevalence of hrHPV among HIV+
women was 45% [42]. Lifestyle factors such as socio-
cultural characteristics, nutritional, environmental, sex-
ual behavior and hygiene, vaginal microbiota and genetic
factors, along with specific geographic distribution of
hrHPV types may explain the varying prevalence of
hrHPV and cervical cancer incidence across populations.
The incidence (52.8 per 100,000) of cervical cancer in
Zambia, East Africa is ~50% higher than in Nigeria,
West Africa where the incidence is 34.5 per 100,000
[18,28,29]. The differences in the prevalent types of
hrHPV in West and East Africa, may partly explain
these regional variations in cervical cancer incidence.
Other studies, like ours, found a high prevalence
of multiple hrHPV infections among HIV+ women
[16,24-27,38,39]. The full spectrum of hrHPV types that
are involved in multiple infections, their persistence, indi-
vidual and relative contribution to oncogenicity and dur-
ation of persistence of the different hrHPV types in the
context of multiple infections in African women is not
known. The etiological and preventative significance of
multiple infections and its potential impact on current
vaccination and HPV DNA based testing strategies are
also not entirely clear and should be assessed in different
populations [16,17].
Differences in epidemiology of hrHPV between devel-
oped and developing countries may be meaningful, given
that the current and next generations of HPV vaccines
do not include some of the types that are prevalent in
Africa. This will be particularly significant if there is little
or no antibody cross-reactivity between current vaccines
and the hrHPV types prevalent in Africa [8]. Given the
high prevalence of non-16 and non-18 hrHPV among
HIV+ women in Nigeria and other African countries,
current vaccines may have limited impact in this section
of the population. Longitudinal investigations of HPV
genotype-specific risks for cervical precancer and cancer
outcomes should be conducted in Africa. As the incidence
of cervical cancer among HIV+ women has increased in
the combination Antiretroviral Therapy era, there is a
need for further studies examining the role of covariates
of persistent hrHPV infection such as sexual behavior, sex-
ual hygiene, diet, smoking, alcohol consumption, concur-
rent genital tract infections, other illnesses and sexual
partner health behavior in cervical carcinogenesis.
Abbreviations
CI: Confidence interval; CIN: Cervical intraepithelial neoplasm; HIV+: HIV
positive; HIV: HIV negative; HPV: Human papillomavirus; hrHPV: high-risk HPV;
IARC: International Agency for Cancer Research; IHVN: Institute of Human
Virology Nigeria; PCR: Polymerase chain reaction; PR: Prevalence ratio.
Competing interests
CMW has received through the University of New Mexico, funds from grants
and cooperative agreements from the US National institutes of Health
related to cervical screening, funds from GSK for HPV vaccine studies and
reimbursements for travel related to publication activities and equipment
and reagents from Roche Molecular Systems for HPV genotyping. Other
authors report no conflicts of interest.
Authors contributions
SNA analyzed the data and drafted the manuscript. MA, AOF, and EOD
contributed to the study coordination. OO and RU, site investigators,
contributed to the study design, implementation and provided revisions of the
manuscript. CMW performed HPV genotyping, contributed to data
interpretation and provided revisions of the manuscript. CAA conceived the
study, obtained funds, contributed to the study design and provided critical
revisions of the manuscript. All authors read and approved the final manuscript.
Acknowledgement
This work was supported by the UM-Capacity Development for Research in
AIDS Associated Malignancy Grant (NIH/NCI 1D43CA153792-01) to CAA. HPV
genotyping was supported by NIAID U19 AI084081 to CMW.
Study design
Cross-sectional survey.
Author details
1
Department of Nutrition, Harvard School of Public Health, 677 Huntington
Avenue, Boston, MA 02115, USA.
2
Office of Strategic Information and
Research Department, Institute of Human Virology Nigeria, 252 Herbert
Macaulay Way, Abuja, Nigeria.
3
Department of Obstetrics and Gynecology,
National Hospital, Abuja, Nigeria.
4
University of Abuja Teaching Hospital,
Gwagwalada, Abuja, Nigeria.
5
Department of Pathology, University of New
Mexico Health Sciences Center, Albuquerque, NM 87131, USA.
6
Institute of
Human Virology and Greenebaum Cancer Center, University of Maryland
School of Medicine, Baltimore, MD 21201, USA.
Received: 8 July 2013 Accepted: 29 October 2013
Published: 5 November 2013
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doi:10.1186/1471-2334-13-521
Cite this article as: Akarolo-Anthony et al.: HIV associated high-risk HPV
infection among Nigerian women. BMC Infectious Diseases 2013 13:521.
Akarolo-Anthony et al. BMC Infectious Diseases 2013, 13:521 Page 6 of 6
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