SERO-prevalence of herpes simplex virus type 1 and type 2 among women attending routine Cervicare clinics in Ghana

Abstract

Background:
Herpes simplex virus infection is a global health concern with disproportionately high burden in low and middle-income countries. There is a paucity of data on the prevalence of HSV infection in Ghana, which necessitated the present study. The aim of the study was to provide up-to-date data on sero-prevalence of HSV-1 and HSV-2 infection among women attending Cervicare clinics in Ghana.

Methods:
This was a cross-sectional study in which 380 women attending routine Cervicare clinics at Regional Hospitals in Kumasi and Accra, Ghana were enrolled into the study. Serum HSV-1 IgG and HSV-2 IgG were determined by ELISA method. The Chi-square test was used to investigate the association between sero-prevalence of HSV-1 and HSV-2 and socio-demographic and behavioral factors using the Statistical Package for the Social Scientists (SPSS) version 22. Statistical significance was accepted at p < 0.05.

Results:
The overall HSV-1 and HSV-2 sero-prevalence estimates were 99.2% (95% CI: 98.0-100%) and 78.4% (95% CI: 74.5-81.8%) respectively. The study observed 78.2% cross-positive prevalence of HSV-1 and HSV-2 among the studied participants. There was no association between the presence of HSV-1 and HSV-2 infection and age (χ2 = 2.351, p = 0.799 and χ2 = 1.655, p = 0.895 respectively). Our findings however, revealed association between the prevalence of HSV-2 and the age at coitarche (p = 0.021) as well as with number of sexual partners (p = 0.022).

Conclusions:
The sero-prevalence estimates of HSV-1 and HSV-2 among the study population of women in Ghana were found to be high. This high prevalence could be attributed to high endemicity and inadequate intervention in this population. There is the need to raise awareness through organized public health screening and education to ensure control.

Full text

R E S E A R C H A R T I C L E Open Access
SERO-prevalence of herpes simplex virus
type 1 and type 2 among women
attending routine Cervicare clinics in Ghana
Oksana Debrah
1,4*
, Francis Agyemang-Yeboah
1
, Richard Harry Asmah
3
, Emmanuel Timmy-Donkoh
1,2
,
Mohammed Mustapha Seini
1,4
, Linda Ahenkorah Fondjo
1
, Nilok Sight
5
and Ellis Owusu-Dabo
2,6
Abstract
Background: Herpes simplex virus infection is a global health concern with disproportionately high burden in low
and middle-income countries. There is a paucity of data on the prevalence of HSV infection in Ghana, which
necessitated the present study.
The aim of the study was to provide up-to-date data on sero-prevalence of HSV-1 and HSV-2 infection among women
attending Cervicare clinics in Ghana.
Methods: This was a cross-sectional study in which 380 women attending routine Cervicare clinics at Regional
Hospitals in Kumasi and Accra, Ghana were enrolled into the study. Serum HSV-1 IgG and HSV-2 IgG were determined
by ELISA method. The Chi-square test was used to investigate the association between sero-prevalence of HSV-1 and
HSV-2 and socio-demographic and behavioral factors using the Statistical Package for the Social Scientists (SPSS)
version 22. Statistical significance was accepted at p<0.05.
Results: The overall HSV-1 and HSV-2 sero-prevalence estimates were 99.2% (95% CI: 98.0–100%) and 78.4% (95% CI:
74.5–81.8%) respectively. The study observed 78.2% cross-positive prevalence of HSV-1 and HSV-2 among the studied
participants. There was no association between the presence of HSV-1 and HSV-2 infection and age (χ
2
=2.351,
p=0.799andχ
2
=1.655,p= 0.895 respectively). Our findings however, revealed association between the prevalence
of HSV-2 and the age at coitarche (p=0.021)aswellaswith numberofsexual partners(p=0.022).
Conclusions: The sero-prevalence estimates of HSV-1 and HSV-2 among the study population of women in Ghana
were found to be high. This high prevalence could be attributed to high endemicity and inadequate intervention in
this population. There is the need to raise awareness through organized public health screening and education to
ensure control.
Keywords: Herpes simplex virus, Sero-prevalence, Ghana
Background
Herpes simplex virus (HSV) has been characterized into
two distinct serotypes: HSV -1 and HSV -2 [1]. HSV
type 1 has been associated with orofacial infections and
HSV type 2 with genital infections. Clinical reports
citing an increasing number of genital infections caused
by HSV -1 have been recognized, although HSV -2
dominates as a causative agent [1,2].
Sixty to 95 % of mature humans are either carrying
HSV viruses or are affected by associated infections
which are usually present in the host in latent state [3].
The large majority of persons with genital herpes do not
know they have the disease. Infection and reactivation
are typically “asymptomatic,”and depend on the host’s
immune system as well as the frequency of entries [3,4].
Both types are highly infectious and can be transmitted
from mother to neonate and increase the mortality rate
[5]. Additionally, infection with HSV-2 increases the risk
of human immunodeficiency virus (HIV) and human
papillomavirus (HPV) acquisition [6,7]. Estimation of
* Correspondence: oksanadeb@yahoo.com
1
Department of Molecular Medicine, Kwame Nkrumah University of Science
and Technology, Kumasi, Ghana
4
Laboratory Department, Ridge Regional Hospital, Accra, Ghana
Full list of author information is available at the end of the article
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International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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the burden of infection is important in appreciating the
scale of the epidemic. Although HSV infection is not a
curable medical condition, there are effective medica-
tions available to treat symptoms and prevent outbreaks.
Unfortunately there is currently no approved vaccine to
prevent HSV infection either [8].
The World Health Organization (WHO) reports that
HSV prevalence shows variations between regions and
populations [9]. The worldwide prevalence of HSV-1
infection in 2012 was 67.0%, with the highest estimated
prevalence of infection in Africa (87%) and lowest in
America (40–50%). The overall prevalence of HSV -2
worldwide was 11.3% [10]. The prevalence of HSV-2 was
consistently higher in females compared to males (14.8
and 8.0% respectively). The highest prevalence was
reported in Sub-Saharan Africa, where prevalence
reached 31.5% followed by America –14.4% [9,10]. In
the meantime, there is a paucity of data on the preva-
lence of HSV infection in Ghana.
The purpose of the study was therefore, to provide
relevant baseline data on sero-prevalence of HSV-1 and
HSV-2 infection and associated risk factors among
women attending routine Cervicare centers in Ghana so
as to inform the development of future studies and guide
public health policy in the context of HSV infections.
Methods
Study design, setting and population
The study was a hospital based cross-sectional descrip-
tive study, covering the period from October 2014 to
March 2015.
In all, three hundred and eighty (380) women attend-
ing routine Cervicare Clinics at the Kumasi South Re-
gional Hospital, Kumasi, Ashanti Region, Ghana and
Ridge Regional Hospital, Accra, Greater Accra Region in
Ghana were enrolled in the study.
The participants were women who had come to Cervi-
care centers for visual inspection with acetic acid or to
perform Papanicolaou (Pap) smear test. The Cervicare
centers were established by Ghana Health Service in
selected regional hospitals and health facilities where
regular public announcements are carried out to invite
the women to participate in screening programs.
Sampling and data collection
Convenient sampling protocols were followed to recruit
the required sample size. The sample size was calculated
by StatCalc application of EpiInfo 3.5.3. The approach
used here to calculate sample size emphasized adequate
precision of reported sample statistics: that is the ability to
estimate sample statistics that do not differ from the true
population parameter by more than a preset limit of confi-
dence. Therefore, assuming a prevalence of HSV of 67%
in the general population of women, and a sufficiently
large population of women attending cervical screening
clinics, a maximum sample size of 340 women ensured
that the study had adequate precision (here we have set
the desired level of precision at ±5%) to provide statistics
close enough to the true population parameters. The
required sample size was pegged at 380 to cater for miss-
ing and incomplete data entries and other unforeseen
circumstances.
To mitigate bias in the sample, researchers conducted
public health awareness campaigns within the catchment
of the hospitals: on radio and at market centers and
encouraged women to present themselves for screening
at no cost. Additionally, a separate day was set aside the
regular clinic days to enroll study participants. At
recruitment, all volunteers gave informed consent by
signature or thumbprint. A questionnaire was adminis-
tered through one-on-one interview for data collection
on socio-demographic and gynecological characteristics,
sexual exposure, medical history and knowledge of HSV
infection. No participants had symptoms of cervical
ulcer from gynecological examination or orofacial ulcer
at the time of recruitment.
Inclusion and exclusion criteria
Participants who were more than 20 years old, non-
pregnant and who had written informed consent and
had gone through a pre-consented interview were in-
cluded in the study. Participants, who were less than
20 years old, had previously undergone a cervical
examination, were pregnant, had refused to sign an in-
formed consent and were unable to undergo a pre-con-
sented interview were not included in the study.
Sample collection
Five milliliters (5 ml) of venous blood was drawn from
all subjects to determine the presence of HSV-1 IgG and
HSV-2 IgG. The samples were allowed to clot before
centrifugation. Serum obtained by centrifugation was
aliquoted into eppendorf tubes for storage at −20° C till
analyzed.
Laboratory analysis
The serum HSV-1 IgG and HSV-2 Ig G were determined
by ELISA method using commercial test kits from
Calbiotech Inc., CA, USA. The manufacturer’s instruc-
tions were followed for the analyses. Briefly, 10 μlof
serum was diluted with 200 μl of diluent and incubated
at room temperature for 5 min. 100 μl of the sample
diluent (as a reagent blank), calibrator, negative and
positive controls, as well as patients’serum were then
aliquoted into microplate wells in duplicate, and incu-
bated at room temperature for 20 min. Three cycles of
washing were performed using 1X washing buffer and
100 μl of anti-IgG conjugate was added and incubated
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for 20 min. The washing procedure was repeated for an-
other three cycles and 100 μl of substrate solution was
added and incubated in the dark at room temperature for
10 min after which the reaction was stopped with 100 μl
of stopping solution. The absorbance was measured at
450 nm within 15 min using a reference wavelength of
600 nm –650 nm. The Antibody (Ab) Index of each de-
termination was calculated by dividing the mean OD value
of each sample as well as negative and positive controls by
the cut-off value. The cut-off value was calculated as
Calibrator OD× Calibrator Factor. Calibrator factor value
was indicated on the calibrator bottle.
Wells with patient antibody index greater than 1.1
were conventionally considered positive for the various
antibodies tested and those between 0.9 and 1.1 were
considered equivocal. While those wells with antibody
index less than 0.9 were considered negative for the
different antibodies tested. All equivocal samples were
retested with reagents of the same kit lot number.
Statistical analysis
The data collected from the questionnaire responses was
stored using Microsoft Excel 2007 software (Microsoft
Corporation, Redmond Campus, Washington DC, USA).
Quantitative variables were tested for normal distribu-
tion and reported as means ± standard deviation. Quali-
tative variables were presented as count (percentages).
The Chi-square test was used to investigate the associ-
ation between sero -prevalence of HSV type 1 and type
2, and socio-demographical and behavioral factors using
the Statistical Package for the Social Scientists (SPSS)
version 22. Statistical significance was conventionally set
at p< 0.05.
Results
Socio-demographic and obstetric characteristics of study
participants
The mean age of study participants was 40.83 years (SD ±
11.12) and ranged from 21 to 76 years. Socio-demographic
characteristics of study participants are presented in Table 1.
The age group from 25 to 44 years was the most repre-
sented (63.2%). Majority of the participants were married
(58.7%). The literacy rate among the women was very high
(91.1%), among which those educated up to the tertiary
level were 22.6% (n= 86), up to SHS/Vocational- 18.1% (n
= 69), up to JHS level- 38.7% (n= 147) and up to primary-
11.6% (n= 44). Majority of women were traders (n=145,
38.2%), self-employed (n= 77, 20.3%) followed by govern-
ment employees (n= 51, 13.4%) and private sector
employees (n= 38, 10.0%).
While about fifth of participants, 19.2% were nullipar-
ous, a large proportion of them had their first pregnancy
between the age of 18–25 years (n= 195, 51.3%)
(Table 2). The study also sought to determine the level
of awareness of women pertaining to HSV and its mode
of transmission (Additional file 1). However, although a
few (n= 37, 9.7%) women had heard about the term
Table 1 Demographics and herpes simplex virus infection sero-
prevalence
Characteristics No
tested
Prevalence of HSV infection
HSV -1 IgG
N (%*)
HSV -2 IgG
N (%*)
Age group, years
≤25 12 12 (3.2) 8 (2.1)
25–34 118 116 (30.5) 94 (24.7)
35–44 122 121 (31.8) 94 (24.7)
45–54 80 80 (21.1) 65 (17.1)
55–64 39 39 (10.3) 30 (7.9)
≥65 9 9 (2.4) 7 (1.8)
χ
2
(df), p- value 2.351
(5), 0.799
1.655
(5), 0.895
Education
Never attended 34 34 (8.9) 30 (7.9)
Primary 44 44 (11.6) 36 (9.5)
Junior High School (JHS) 147 146 (38.4) 128 (33.7)
Senior High School (SHS) 45 45 (11.8) 30 (7.9)
Technical/ vocational 24 24 (6.3) 16 (4.2)
Tertiary 86 84 (22.1) 58 (15.3)
χ
2
(df), p- value 3.783
(5), 0.581
20.500
(5), 0.001
Marital status
Never married 61 59 (15.5) 45 (11.8)
Divorced/separated 33 33 (8.7) 29 (7.6)
Married 223 222 (58.4) 174 (45.8)
Cohabiting 31 31 (8.2) 23 (6.1)
Widowed 32 32 (8.4) 27 (7.1)
χ
2
(df), p- value 5.921
(4), 0.205
3.542
(4), 0.472
Occupation
Government employee 51 50 (13.2) 39 (10.3)
Private sector employee 38 37 (9.7) 30 (7.9)
Self -employed 77 76 (20.0) 50 (13.2)
Trader 145 145 (38.2) 128 (33.7)
Subsistence farming 4 4 (1.1) 4 (1.1)
Student 12 12 (3.2) 8 (2.1)
House wife 5 5 (1.3) 3 (0.8)
Unemployed 35 35 (9.2) 26 (6.8)
Retired 13 13 (3.4) 10 (2.6)
χ
2
(df), p- value 4.498
(8), 0.810
20.172
(8), 0.010
*- Column percentages computed in relation to total number of women (380)
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Herpes, none of the women knew about HSV or its
mode of transmission.
Sero-prevalence of study participants
The overall HSV-1 and HSV-2 sero-prevalence were
99.2% (95% CI: 98.0–100.0%) and 78.4% (95% CI: 74.5–
81.8%) respectively (Tables 3and 4). The majority of sero-
positive participants for HSV-1 and HSV-2 were between
25 and 44 years (n= 237), and the least rates were among
those 65 years and older (n=9)(Table1). Chi-square ana-
lysis did not indicate any association between the occur-
rences of HSV-1 and HSV-2 infection and age groups (χ
2
=2.351, p= 0.799 and χ
2
=1.655, p= 0.895 respectively).
Overall, sero-prevalence of both types of herpes infection
did not differ by marital status of participants (p=0.205
for HSV-1 and p= 0.472 for HSV-2). A strong association
existed between HSV-2 infection and level of education
among participants (p= 0.001) and the age of first
pregnancy (p=0.003), but not in the case of HSV-1 infec-
tion (p= 0.581 and p= 0.086 respectively).
The study observed that cross-positive prevalence of
HSV-1 and HSV-2 of study participants was 78.2% (95%
CI: 73.9–81.6%). There was no association between
multiple infection and age of participants (χ
2
= 6.702, p
= 0.753), as the same in case of marital status (χ
2
=
13.531, p= 0.095). A study also showed a strong associ-
ation between multiple infection and educational status
(p= 0.006) and the age of first pregnancy (p= 0.001).
Sexual risk factors
The analysis of some behavioral risk factors associated
with HSV-1 and HSV-2 sero-prevalence is presented in
Table 5. There were significant differences between
number of sexual partners and the prevalence of HSV-2
(p= 0.022). A higher proportion of women (57.9%) had
the first sexual relationship before age 20. The study
showed that the prevalence of HSV-2 decreased as the
age at coitarche increased. This association was statisti-
cally significant (p= 0.021). Multiple infection was
associated with age of first sexual debut (p= 0.004), but
not with multiple sexual partners (p= 0.137).
Discussion
There is a paucity of data on sero-prevalence of HSV
infection type 1 and type 2 in Ghana. To our knowledge
this is the first study on sero-prevalence of HSV-1 and
Table 2 Obstetric characteristics and herpes simplex virus
infection sero-prevalence
Characteristics No.
tested
Prevalence of HSV infection
HSV 1 IgG N (%*) HSV 2 IgG N (%*)
Age at first pregnancy, years
≤17 36 35 (9.2) 29 (7.6)
18–21 98 98 (25.8) 86 (22.6)
22–25 97 96 (25.3) 81 (21.3)
> 25 72 72 (18.9) 53 (13.9)
Never pregnant 45 43 (11.3) 27 (7.1)
Do not remember 32 32 (8.4) 22 (5.8)
χ
2
(df), p- value 9.641 (5), 0.086 17.840 (5), 0.003
Gravidae
0 45 43 (11.3) 27 (7.1)
1–2 90 90 (23.7) 72 (18.9)
3–4 133 132 (34.7) 109 (28.7)
≥5 112 112 (29.5) 90 (23.7)
χ
2
(df), p- value 9.285 (3), 0.026 10.386 (3), 0.016
*Column percentages computed in relation to total number of women (380)
Table 3 Sero-prevalence of HSV-1 IgG and HSV-2 IgG among
the study participants
Result HSV-1 IgG HSV-2 IgG
N (%) N (%)
Positive 377 (99.2) 298 (78.4)
Borderline 1 (0.3) 54 (14.2)
Negative 2 (0.5) 28 (7.4)
Table 4 HSV-1 IgG and HSV-2 IgG positivity stratified by ELISA
OD index
Result HSV-1 IgG HSV-2 IgG
N (%) N (%)
Low positive 228 (60.0) 203 (53.4)
High positive 149 (39.2) 95 (25%)
Low positiv e: 1.1 < OD ≤2.0; High positive: OD > 2.0
Table 5 Study population behavioral factors and herpes
simplex virus infection sero-prevalence
Characteristics No.
tested
Prevalence of HSV infection
HSV 1 IgG N (%*) HSV 2 IgG N (%*)
Age of coitarche, years
≤15 28 28 (7.4) 23 (6.1)
16–20 192 192 (50.5) 157 (41.3)
21–25 53 51 (13.4) 38 (10.0)
≥26 24 24 (6.3) 13 (3.4)
Do not remember 83 82 (21.6) 67 (17.6)
χ
2
(df), p- value 8.150 (4), 0.086 11.521 (4), 0.021
Number of life time sex partners
1 155 154 (40.5) 110 (28.9)
2 91 90 (23.7) 73 (19.2)
3–9 127 126 (33.2) 109 (28.7)
10+ 7 7 (1.8) 6 (1.6)
χ
2
(df), p- value 0.208 (3), 0.976 9.598 (3), 0.022
*Column percentages computed in relation to total number of women (380)
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HSV-2 infection among the women presenting to
Cervicare centers in Ghana. The study showed a high
prevalence of HSV-1 and HSV-2 among the population
of women (99.2 and 78.4% respectively).
Our findings are consistent with those of studies
among various populations in several African countries
[9]. A study conducted among women in urban Uganda
and among pregnant women in Benin city of Nigeria
also showed very high prevalence of HSV-1 infection: 98
and 96.6% respectively [11,12] whereas prevalence of
HSV-1 infection among pregnant women in Vanuatu
was reported as 100% [13]. In 2012, the WHO 2012
reported a global prevalence of HSV-1 of 68%, with the
highest prevalence in Africa (87%) [9].
In the case of HSV-2 infection our findings are corrob-
orated by other studies conducted in Ghana [14,15].
Those studies focused on smaller numbers of partici-
pants. One of the studies showed a sero-prevalence of
HSV-2 infection among women attending sexually trans-
mitted disease (STD) clinics in Accra and Kumasi
(Ghana) of 71% (n= 278) [14]. The other study
conducted in Ghana among 91 pregnant women also
reported a high prevalence of HSV-2 (68%) which is
similar to the current findings [15].
Similar high sero-prevalence rates have been reported
in other African countries. Among pregnant women in
Cote D’Ivoire −96.5% [16], women attending STD clinics
in Bangui (Central Africa Republic) and Nigeria: 95 and
86.4% respectively [14,17]. The high prevalence of
HSV-2 infection on our study could be due to the high
transmission of the virus. The lack of awareness of this
viral infection among the population and environmental
factors could also be contributory factors.
However, the prevalence of HSV-2 was higher com-
pared to estimates from some African studies as well.
The prevalence of infection among women was 58% in
Uganda [11], 68% in Zimbabwe [18], 55% in Zambia [19]
and 28% in Gambia [20]. A study conducted in Sudan
among pregnant women reported a prevalence rate of
34.6% for HSV-2 infection [21] and 20.7% in Tanzania
[22]. Two independent studies from Nigeria reported
lower sero-prevalence of HSV-2 infection among preg-
nant women, 44.3% [12] and 47.3% [23] than we found.
HSV-2 prevalence is thought to increase with age as
infection is lifelong [10]. However, our study did not re-
veal a significant correlation between age and HSV-2
infection. This finding was also observed in a study
conducted among Sudanese pregnant women [21]. The
sexual behavioral factors associated with HSV-2 were
young age at sexual debut and multiple sexual partners.
Other research supports our findings that earlier age of
sexual intercourse is associated with prevalence of
HSV-2 infection. Our findings correlated with those
reported in Nigeria, India and Zimbabwe [23–25].
Some studies had also indicated that HSV-2 infection
is associated with multiple sex partners [24]. In our
study this behavioral factor was also significantly associ-
ated with HSV-2 prevalence (p= 0.022).
However, the presence of HSV-1 infection was not
related to sexual behavior in this study. This could be
because women in our study were infected early in life
and already had antibodies against HSV-1 by the time
they became sexually active. This is corroborated by a
report from WHO, where in Africa and South-East Asia
most HSV-1 infection occurred during first 5 years of
life, with no new infections in adulthood [9].
The high estimate of HSV infection highlights the
need for development of vaccines and other new HSV
prevention strategies [10].
In general, there was very low awareness of the clinical
symptoms and mode of transmission of the HSV infec-
tion among the women enrolled in the study. Some even
believed that, lesions around the mouth were symptoms
of malaria. Even though herpes infection could look
harmless (since the infected person may be asymptom-
atic and clueless) it is a lifelong infection which could
lead to a “silent”spread in the population, with possible
debilitating consequences. This implies that public
health concern should be seriously directed to this issue
in Ghana. There is a necessity for educational programs
and improved strategies in patient care, especially in
at-risk populations.
Limitations
The study design used in this work may limit the
generalizability of these findings to the broader popula-
tion because of variability in risk factor profiles among
the general population of women and women with
health seeking behavior. Because of this, it is possible
that prevalence estimates reported here may be slightly
higher than in the general population. Any attempt to
generalize these studies beyond this population must be
made with caution. Nevertheless, we conducted public
health awareness campaigns within the catchment of the
hospitals: on radio and at market centers and encour-
aged women to freely present themselves for screening
at no cost. Additionally, it is hoped that fixing a separate
day aside the regular clinic days to enroll study partici-
pants could arrest and mitigate any bias. Also, because
these results are based on cross-sectional data, any
causal inference is speculative.
Conclusion
The prevalence of HSV-1 and HSV-2 among the women
attending the Cervicare centers in Accra and Kumasi,
the two major cities in Ghana was high. The major fac-
tor found to be associated with sero-prevalence of
HSV-2 was age at coitarche and number of life time
Debrah et al. BMC Infectious Diseases (2018) 18:378 Page 5 of 7
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sexual partners. This could be due to the high endem-
icity and inadequate intervention in this population, the
lack of awareness of some viral infections among the
population and environmental factors. There is the need
to raise awareness through organized public health
screening and education to ensure control.
Additional file
Additional file 1: Questionnaire. (DOCX 19 kb)
Abbreviations
HIV: Human Immunodeficiency Virus; HPV: Human Papillomavirus;
HSV: Herpes Simplex Virus; JHS: Junior High School; Pap: Papanicolaou;
SHS: Secondary High School; SPSS: Statistical Package for the Social Scientists;
WHO: World Health Organization
Acknowledgements
We wish to acknowledge all the staff of Cervicare centers from both facilities
(Accra and Kumasi) in Ghana and all the study participants.
Ethical approval and consent to participate
The study was approved by the Committee on Human Research Publication and
Ethics (CHRPE), Kwame Nkrumah University of Science and Technology, School of
Medical Sciences (KNUST-SMS) and Komfo Anokye Teaching Hospital (KATH)
(CHRPE/AP/115/14), Kumasi, Ghana and Ghana Health Service Ethical Review
Committee, Research and Development Division (GHS-ERC:07/03/14). Voluntary
written informed consent was sought from the participants. The study was
conducted in an environment with no form of coercion and volunteers were
adequately informed of the purpose, nature and procedures of the study.
Availability of data and materials
The datasets used and/or analyzed during the current study are available
from the corresponding author on reasonable request.
Authors’contributions
OD formulated the concept, carried out the implementation of the research,
involved in the recruitment of the participants and data collection, performed
laboratory analysis, analyzed and interpreted the data, wrote the manuscript
with input from all authors. FAY formulated the concept, directed the
implementation of research, supervised findings of this work, and was a major
contributor in writing the manuscript and final approval of the version to be
published. RHA help to supervise the project and contributed to the final
version of the manuscript. ETD involved in the recruitment of the participants
and data collection, contributed to the analyses of the results and to
the final version of the manuscript. MMS assisted with laboratory analysis
and contributed to the final version of the manuscript. LAF contributed to the
final copy of the manuscript. NS assisted with laboratory analysis and contributed
to the final version of the manuscript. EOD supervised the project and
contributed to the final version of the manuscript. All authors read and
approved the final manuscript.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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Author details
1
Department of Molecular Medicine, Kwame Nkrumah University of Science
and Technology, Kumasi, Ghana.
2
Kumasi Center for Collaborative Research
in Tropical Medicine, Kwame Nkrumah University of Science and Technology,
Kumasi, Ghana.
3
College of Health Sciences, University of Ghana, Legon,
Accra, Ghana.
4
Laboratory Department, Ridge Regional Hospital, Accra,
Ghana.
5
Laboratory Department, C&J Medicare Hospital and Diagnostic
Center, Accra, Ghana.
6
Department of Global Health, School of Public
Health,KNUST, Kumasi, Ghana.
Received: 19 September 2017 Accepted: 31 July 2018
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