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Cervical Human Papillomavirus Prevalence, Genotypes, and Associated Risk Factors among Female Sex Workers in Greater Accra, Ghana

Cervical Human Papillomavirus Prevalence, Genotypes, and Associated Risk Factors among Female Sex... Hindawi Journal of Oncology Volume 2019, Article ID 8062176, 7 pages https://doi.org/10.1155/2019/8062176 Research Article Cervical Human Papillomavirus Prevalence, Genotypes, and Associated Risk Factors among Female Sex Workers in Greater Accra, Ghana 1 2 3 Abdul Rashid Adams, Priscillia Awo Nortey, Benjamin Ansah Dortey, 1 4 Richard Harry Asmah , and Edwin Kwame Wiredu Department of Medical Laboratory Sciences, School of Biomedical and Allied Health Sciences, College of Health Sciences, University of Ghana, Korle-Bu, Accra, Ghana School of Public Health, College of Health Sciences, University of Ghana, Legon, Accra, Ghana Trauma Hospital, Winneba, Ghana Department of Pathology, School of Biomedical and Allied Health Sciences, College of Health Sciences, University of Ghana, Korle-Bu, Accra, Ghana Correspondence should be addressed to Edwin Kwame Wiredu; ekwiredu@chs.edu.gh Received 7 March 2019; Accepted 14 May 2019; Published 2 June 2019 Guest Editor: Hisashi Iizasa Copyright © 2019 Abdul Rashid Adams et al. is Th is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Cervical cancer is a largely preventable disease mediated by persistent infection with high-risk Human Papillomaviruses (Hr-HPV). There are now three approved vaccines against the most common HPV genotypes. In Ghana, mortality due to cervical cancer is on the rise, due to the absence of an organized and effective cervical cancer prevention and control program. Data on circulating HPV genotypes is important for studying the likely impact of mass introduction of HPV vaccination of the female population before sexual debut. High HPV prevalence has been reported in Female Sex Workers (FSWs), who constitute an important active group for maintenance of HPV in the population. is Th study was conducted to determine the size of HPV prevalence in this group and to provide information for future assessment of the impact of vaccine introduction in the country. We conducted a cross-sectional study where the snowballing technique was used to identify and select FSW’s≥18 years, operating within suburbs of Greater Accra Region (GAR). A risk factor assessment interview was conducted and cervical swabs were collected for HPV-DNA detection and genotyping by Nested Multiplex PCR. Hundred participants, age ranging from 18 to 45 years, median 24 years, were studied. eTh prevalence of Cervical HPV was 26%. Eleven genotypes were detected comprising 9 high-risk in order of decreasing prevalence HPV-16 (8%), HPV-35 (5%), HPV-33/39/-68 (3%), HPV-52/51/59 (2%) and HPV-18 (1%) and 2 Low-risk types, HPV-42(3%), and HPV-43 (1%). rTh ee women had HPV types that could not be genotyped by our method. Oral contraceptives use was associated with a reduced chance of HPV infection (P=0.002; OR=0.19, 95% CI 0.07-0.54). is Th study found a high HPV prevalence among FSWs in the GAR. A high number of Hr-HPV genotypes seen are vaccine preventable, providing additional compelling argument for implementing a national cervical cancer prevention plan including vaccination. 1. Introduction common female malignancy [3]. In Ghana, it is likely the commonest cancer among women. Current estimates indi- Globally, cervical cancer remains a primary cause of mor- cate that every year 3,151 women are diagnosed with cervical bidity and mortality, with estimated 569,847 new cases and cancer and 2,119 die from the disease in the country [4]. 311,365 attributable deaths in 2018 [1, 2]. The highest incidence Infection of the cervix by a high-risk Human Papillo- has been reported in low and middle income countries, mavirus (HPV), a common sexually transmitted infection, is necessary for the development of cervical cancer [5] particularly in Sub-Saharan Africa where it is the second most 2 Journal of Oncology Many studies have found a direct association of HPV containing DNAgard (Biomatrica, San Diego, CA, USA) for infection with sexual behaviour and have indicated that HPV-DNA detection and genotyping. Samples were collected a high number of lifetime partners may lead to a higher by single use, disposable equipment. transmission of HPV leading to higher cervical cancer rates [6–8]. 2.3. HPV Testing. HPV detection and typing were carried out Female sex workers (FSWs) are a group of females who by Nested multiplex PCR. [10]. A single consensus forward provide sexual services for economic remuneration. Due to primer (GP-E6-3F) and two consensus back primers (GP- exposure to multiple sexual partners in their occupation, E7-5B and GP-E7-6B) were used for HPV DNA detection they are prone to various sexually transmitted infections, in the rfi st round PCR. The PCR reaction mix of 25 𝜇 l including HPV. Sexual contact with FSWs plays an important contained 10X PCR buffer, 2.5mM MgCl 200𝜇 Mofeach role in HPV transmission and might be a major contributor of the four deoxyribonucleoside triphosphates (dNTP’s), to the prevalence of HPV and cervical cancer among women 15pmols of each E6/E7 consensus primers, and 1.25 units in the general population. Also, through the transmission of of Taq polymerase enzyme. Five microliters (5𝜇 l) of DNA the virus to their male clients, they increase the risk of penile extracts was used as a template for the amplification reactions cancers among these men [9]. Furthermore, due to their likely using a thermal cycler (Robocycler Gradient 96, Strategene, interaction with foreign clients and sex tourists, they may USA). The cycling parameters for the rfi st round PCR with possibly havea role in thegenotypediversity of HPV in the E63F/E75B/E76B consensus primers were as follows: 94 Cfor country. four minutes, followed by 40 cycles of 94 C for one minute, ∘ ∘ In Ghana, mortality due to cervical cancer is on the 40 Cfor two minutes, 72 C for two minutes, and a single final rise, most likely due to the lack of an organized preven- elongation step of 72 C for 10 minutes. In the second round tion and control program. Information on circulating HPV PCR, Primers for the identicfi ation of high-risk genotypes 16, genotypes is crucial for determining the impact of cervical 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, and 68 and low-risk cancer control programmes, including HPV immunization. genotypes 6/11, 42, 43, and 44 were used. The primers were The high rates of HPV reported among FSWs make them used in four cocktails, each containing four to vfi e different a priority group for study as we seek to characterize the primer pairs. Two microliters of first round PCR product, 15 prevalent HPV genotypes in the country in order to predict pmols of forward, and reverse primers for genotyping were the likely impact of the current vaccines in reducing the used. The other parameters remained the same as used in incidence of cervical cancer after introduction of mass female the rfi st round PCR. However, the cycling parameters were as ∘ ∘ vaccination in the country. The study also looked at other follows: 94 C for four minutes followed by 35 cycles of 94 C ∘ ∘ factors that may increase the risk of HPV, contribute to for 30 seconds, 56 Cfor 30 seconds, 72 Cfor 45 seconds, and persistence of infection, and/or promote progression of HPV- a single final elongation step of 72 Cfor four minutes [10]. induced changes in the cervical epithelium. Here, we report Positive and negative controls were included in each round the rfi st study of cervical HPV and its associated risk factors of amplicfi ation. among FSW’s in Ghana. The amplicons were resolved on 2% agarose gel stained with 0.5𝜇 g/ml ethidium bromide. Ten microliters of each sample was added to 2𝜇 lof orange G (10X) gel loading dye 2. Methods for the electrophoresis. Hundred base pair DNA molecular 2.1. Study Design and Population. This was a cross-sectional weight marker (Sigma, MO, USA) was run alongside the study undertaken between February and July 2016 in Greater PCR products. The gel was prepared and electrophoresed Accra, one of the ten administrative regions of Ghana in 1X TAE buffer using an electrophoresis tank at 80 volts (and which houses the national capital) with a predomi- for one hour and the gel photographed over an Ultraviolet nantly urban population. A risk factor assessment interview (UV) transilluminator [10]. HPV genotypes were identified was conducted for 100 out of the 109 FSWs who were by comparing the molecular weight of the bands observed to reached through snowballing, to elicit data on their basic positive control band and or the expected amplicon sizes in demographics, sexual activities and behaviours (including each primer cocktail. the age of sexual debut), reproductive history, menarche, sexually transmitted disease (STD) history, screening his- 2.4. Data Analysis. The data obtained through the question- tory, and smoking habit (past and present). Only FSWs naire was checked for accuracy and entered into the computer of age 18 years and above and had been a sex worker for using Microsoft Excel (2016) Programme and was analysed at least 6 months were included in the study. The Ethics using SPSS version 20 (IBM Corp. Armonk, New York, USA). and Protocol Review Committee of School of Biomedical Exploratory analysis was first carried out to obtain descriptive and Allied Health Sciences, University of Ghana, approved statistics. Charts and tables were used to summarize data and this study (SBAHS/10161447/AA/MLS/2015-2016). Partici- display gfi ures where appropriate. The number and propor- pants were fully informed about the purpose, procedures, tion of HPV DNA positives and type-specific HPV infection risks, and benefits of participating in this study and Informed were calculated. To assess the association between HPV DNA consent was obtained from all subjects. positivity and sociodemographic and sexual behavioural factors, odds ratios (ORs) and 95% CIs were calculated using 2.2. Specimen Collection. Following the interviews, a Gynae- logistic regression. In all statistical considerations a p-value cologist collected exfoliated cells from the cervix into tubes <0.05 was considered statistically significance. Journal of Oncology 3 <25 25-34 35-44 45-54 Age group Prevalence Figure 1: Age-specific HPV prevalence. 3. Results 17% (17/100) (Figure 1). Of the HPV positive women, 73.1% (19/26) were infected with only high-risk types, 3.9% (1/26) 3.1. Participant Characteristics. A total of 100 FSW, ages were with only low-risk types, and 11.5% (3/26) had both ranging from 18 to 45 years with a median age of 24 years, high- and low-risk types. were interviewed. More than half (58%) of them were below Table 2 shows the cytological changes found in the high- 25 years. The level of education among the women was risk HPV cases detected with 3 cases each of ASCUS, LSIL, generally low, with the vast majority, 74% (74/100), having and HSIL. at most basic education while 6% (6/100) reported to be illiterates. The median length of sex work was 2 years with 3.3. Risk Factors for HPV Infection. To identify putative risk a range of 0.5-26 years. About a half (53%) of the sex workers factors for HPV infection, we performed univariate regres- reported engaging in other economic activities (mostly petty sion analysis and the results are presented in Table 3. HPV trading) while the rest (47%) were full time sex workers. infection was found not to be significantly associated with, Seventy-seven percent of the subjects who remember their age, education, smoking, average number of clients per week, age at sexual debut recalled it to be≥16 years and 59% of them previous sexual disease, condom use, age at sexual debut, had at least a child. Condom use always was reported by 82% and parity. In contrast, the use of oral contraceptives was (82/100) of the study participants whereas oral contraceptive the only variable that significantly influenced HPV Infection use was reported by 20%. Two (2%) subjects reported to be (P=0.002). Female sex workers who used oral contraceptives HIV positive while 14/100 (14%) had had gonorrhoea, 4/100 had 19% reduced odds of having HPV infection compared to (4%) syphilis, 3/100 (3%) genital warts, and 2/100 (2%) herpes those who did not (OR=0.19, 95% CI 0.07-0.54). before. A third (33%) of them had ever smoked cigarette whist 17% are active smokers. Only 9/100 (9%) had ever undergone 4. Discussion cervical cancer screening. Studies have indicated that a high number of lifetime partners 3.2. HPV Prevalence and Genotypes. The overall HPV preva- may lead to a higher transmission of HPV [6, 7]. The nature lence (any HPV) was 26% (26/100). Eleven genotypes were of work conducted by sex workers predisposes them to an detected comprising 9 high-risk types and 2 low-risk types. increased risk of HPV infection. This study found a crude The high-risk HPV types in order of decreasing preva- HPV prevalence of 26% among female sex workers in the lence were HPV-16 (8%; 8/100), HPV-35 (5%; 5/100), HPV- Greater Region, which is higher than the WHO estimate of 33/39/68 (3%; 3/100), and HPV-51/52/59 (2%; 2/100) HPV- 19.5% HPV Prevalence in women from Western Africa at a 18 (1%;1/100). HPV 42, (3%; 3/100) and HPV-43 (1%; 1/100) given time [3]. This is consistent with existing reports of the were the low-risk HPV types found. In addition 3% (3/100) elevated HPV prevalence in Female sex workers compared had HPV that could not be typed by our method (Table 1). to womeninthegeneralpopulation. Similar studies in There were 21% single HPV infections (including the three other African countries have shown much higher prevalence: that we could not type) and 5% multiple HPV infections. The Madagascar (36.7) among 90 FSWs [11], Senegal (43.5%) 5 multiple infections comprised two each of quadruple- and among 681 FSWs [12], Tunisia (39.2%) among 51 FSWs [13], double-infections and one triple infection. The highest HPV Burkina Faso (66.1%) among 360 FSWs [14], Kenya (55.6%); infection rate was among women aged below 25 years with among 789 FSWs [15], South Africa (62.6%), among 99 HPV Prevalence 4 Journal of Oncology Table 1: Type-specific HPV prevalence. HPV type Single infections Multiple infections Total (%) n=100(100) High-risk infections 16 4 4 8(8) 35 4 1 5(5) 33 2 1 3(3) 39 3 0 3(3) 68 1 2 3(3) 51 2 0 2(2) 52 1 1 2(2) 59 2 0 2(2) 18 0 1 1(1) sub-total 19 10 29(29) Low-risk infections 42 2 1 3(3) 43 0 1 1(1) sub-total 2 2 4(4) Un-typeable X3 0 3(3) Total (LR+HR+X) 24 12 36(36) Table 2: Cytologic changes in HR-positive individuals. (NMPCR) [10] to the conventional PCR (with either MY09- MY11 or GP5+-GP6+ primers) utilized in some of the studies Cytology results HR-Genotypes above, we recorded a lower HPV prevalence compared to NILM 16, 18, 68 those studies. This may likely be due to the fact that 36% NILM 16,35,68 of the FSWs from the Burkina Faso study, 35.2 % from the NILM 33 Kenya study, and 50.3% from the South African study were HIV positive compared to the very low 2% in this study. NILM 39 Cervical HPV infections are substantially more common HSIL 16,33,68 among women infected with HIV, compared with HIV- NILM 52 uninfected women with similar sexual histories due to their NILM 35 impaired immunity and this has been reported by several NILM 16 studies [18–20]. NILM 16 A high number of HPV positive FSWs (17/26), though not NILM 16 statistically significant, were below 25 years. This is consistent NILM 39 with reports in a global review of HPV prevalence among LSIL 16 female sex workers [8]. This observation may be linked with LSIL 35 acquisition of high rates of HPV following commencement ASCUS 51 of sex work. Secondly, this may be related to power play as older sex workers are better able to negotiate condom HSIL 51 use than younger sex workers, although condom use does NILM 35 not provide full protection from HPV infection. This could HSIL 39 also be ascribed to young sex workers enticing more clients ASCUS 16,52 than older sex workers culminating in an increased rate of NILM 35 exposure to HPV. It is however worth stating that more than LSIL 33 half (58%) of our study subjects were within this age bracket NILM 59 and therefore this age trend could have also been due to this ASCUS 59 selection bias. The high-risk HPV genotypes detected in decreasing order of prevalence were 16 (8%), 35 (5%), 33/39/68 (3%), FSWs [16]. These variations could be due to difference in 51/52/59 (2%), and 18 (1%). These genotypes are similar to sampling strategies and HPV assays employed [17] besides what is seen in studies in Ghanaian women with and without cervical cancer and elsewhere in Africa but with vary- risk factors which are known to vary by region. Though we employed a comparatively more sensitive HPV assay ing individual genotype prevalence [21–25]. About 50% of Journal of Oncology 5 Table 3: Results of univariate logistic regression analysis of risk factors for HPV infection. Variables HPV (+) HPV (-) OR (95% CI) P-value Age(years) <25 17 41 0.65 (0.26- 1.67) 0.38 25-34 3 23 3.46 (0.9412.67) 0.06 35-44 6 9 0.46 (0.15-1.46) 0.19 45-54 0 1 - - Education No formal education 1 5 1.81 (0.20-16.27) 0.60 Basic 18 56 1.38 (0.52-3.71) 0.52 Higher 7 13 0.59 (0.20-1.66) 0.31 Time in prostitution (years) <1 6 17 1.45(0.48-4.38) 0.51 1-2 6 27 1.47(0.55-3.94) 0.46 3-4 6 13 0.65(0.21-1.94) 0.44 ≥5 8 15 0.58(0.20-.1.65) 0.31 Full time sex worker Yes 13 34 0.85 (0.35-2.08) 0.72 Average clients per week ≤14 14 40 1.01 (0.41-2.71) 0.99 >14 12 34 1.05 (0.43-2.66) 0.92 Contraceptive Condom 20 62 1.55 (0.52-4.66) 0.44 Oral contraceptive 11 9 0.19(0.07-0.54) 0.002∗ Age at sexual debut(yrs.) <16 7 16 0.74 (0.27-2.09) 0.58 16-20 19 55 1.07 (0.38-2.93) 0.90 >20 0 3 - 0.99 No. of Children 0 11 30 0.93 (0.37-2.30) 0.88 1-2 14 36 0.81 (0.33-1.99) 0.65 ≥3 1 8 3.03 (0.36-25.47) 0.31 Smoking History Current smoking 7 10 0.42 (0.14-1.26) 0.12 Past smoking 9 24 0.91 (0.35-2.32) 0.84 STI in the past Yes 9 14 0.44(0.16-1.11) 0.11 Past STI type Genital warts 1 1 0.34(0.02-5.68) 0.46 Gonorrhoea 5 9 0.58(0.12-5.68) 0.36 Syphilis 2 2 0.33(0.04-2.50) 0.29 Herpes 1 1 0.34(0.02-5.68) 0.46 HIV 2 0 - - high-risk-HPV genotypes detected in this study are covered country even after the institution of a national vaccination by the Nona-valent vaccine (Gardasil 9, Merck) [26] and policy. For example, HPV-35, the second most common therefore the introduction of this vaccine and ultimately a HPV type found in this study, is not a vaccine type. In national vaccination policy would positively impact cervical another study conducted in Ghana among HIV seropositive prevention eor ff ts in the country. However, the fact that not and negative women, HPV-35 was the commonest genotype all high-risk-HPV detected in this and several other studies detected and was significantly associated with Squamous in Ghanaian women with and without cervical cancer are intraepithelial lesions [25]. The low-risk-HPV genotypes vaccine types means cervical screening will continue to play detected, in decreasing order of prevalence, were 42 and 43. an important role in cervical cancer prevention eo ff rts in the These two genotypes were the two common low-risk types 6 Journal of Oncology detected in a study involving pregnant women attending Kwame Wiredu were responsible for design, data generation, antenatal clinic at the Korle-Bu teaching hospital in Accra and data analysis. Abdul Rashid Adams, Richard Harry [23]. Asmah and Edwin Kwame Wiredu took care of manuscript Oral contraceptives use significantly influenced HPV Development. All authors critically reviewed and approved infection (P=0.002), with about 19% decreased chance of the final manuscript. HPV infection in oral contraceptive users compared to nonusers (OR=0.19, 95%CI 0.07-0.54). However, a systematic Acknowledgments review of 19 epidemiological studies of the risk of genital The authors would like to thank all those who agreed to HPV infection and oral contraceptive use concluded that take part in the study, Mr Clement Azigwe, Miss Ramatu, there was no evidence for a strong positive or negative and Sister Janet for their tremendous help in recruiting association between HPV positivity and ever use or long the study subjects. They are grateful to the management duration use of oral contraceptives [27]. There was lack of and staff of All Faith Medical Centre, for allowing their significant association of HPV infection with known risk facility to be used for sample collection and interviews. factorssuchassmoking,ageatsexualdebut,numberofsexual They also deeply appreciate the contributions of Mr. Maxwell partners, and history of STI. These findings could be due Akanburichab, Ms. Kathleen Korkor Glover, Mrs. Lois Botwe, to the small sample size and/or the reliability or otherwise and Mr. Bright Katey of all department of Medical Laboratory of the information provided by the study subjects. The risk science, University of Ghana, during the sample collection factors assessed in this study relied on self-reported data and and interviews. therefore prone to both recall and social appeal bias. Thisisthe rfi st report of cervical HPVand associated References risk factors among FSW’s in Ghana. Our study also has some limitations: this study was done on a small scale; therefore [1] J. Ferlay, M. Ervik, F. Lam et al., Global Cancer Observatory: a larger study with a higher statistical power is needed to Cancer Today, International Agency for Research on Cancer, determine the extent of HPV infection in this population. Lyon, France, 2018. Also, the convenience sampling method employed means the [2] L.Bruni,L. 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Cervical Human Papillomavirus Prevalence, Genotypes, and Associated Risk Factors among Female Sex Workers in Greater Accra, Ghana

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Hindawi Publishing Corporation
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Copyright © 2019 Abdul Rashid Adams et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2019/8062176
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Hindawi Journal of Oncology Volume 2019, Article ID 8062176, 7 pages https://doi.org/10.1155/2019/8062176 Research Article Cervical Human Papillomavirus Prevalence, Genotypes, and Associated Risk Factors among Female Sex Workers in Greater Accra, Ghana 1 2 3 Abdul Rashid Adams, Priscillia Awo Nortey, Benjamin Ansah Dortey, 1 4 Richard Harry Asmah , and Edwin Kwame Wiredu Department of Medical Laboratory Sciences, School of Biomedical and Allied Health Sciences, College of Health Sciences, University of Ghana, Korle-Bu, Accra, Ghana School of Public Health, College of Health Sciences, University of Ghana, Legon, Accra, Ghana Trauma Hospital, Winneba, Ghana Department of Pathology, School of Biomedical and Allied Health Sciences, College of Health Sciences, University of Ghana, Korle-Bu, Accra, Ghana Correspondence should be addressed to Edwin Kwame Wiredu; ekwiredu@chs.edu.gh Received 7 March 2019; Accepted 14 May 2019; Published 2 June 2019 Guest Editor: Hisashi Iizasa Copyright © 2019 Abdul Rashid Adams et al. is Th is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Cervical cancer is a largely preventable disease mediated by persistent infection with high-risk Human Papillomaviruses (Hr-HPV). There are now three approved vaccines against the most common HPV genotypes. In Ghana, mortality due to cervical cancer is on the rise, due to the absence of an organized and effective cervical cancer prevention and control program. Data on circulating HPV genotypes is important for studying the likely impact of mass introduction of HPV vaccination of the female population before sexual debut. High HPV prevalence has been reported in Female Sex Workers (FSWs), who constitute an important active group for maintenance of HPV in the population. is Th study was conducted to determine the size of HPV prevalence in this group and to provide information for future assessment of the impact of vaccine introduction in the country. We conducted a cross-sectional study where the snowballing technique was used to identify and select FSW’s≥18 years, operating within suburbs of Greater Accra Region (GAR). A risk factor assessment interview was conducted and cervical swabs were collected for HPV-DNA detection and genotyping by Nested Multiplex PCR. Hundred participants, age ranging from 18 to 45 years, median 24 years, were studied. eTh prevalence of Cervical HPV was 26%. Eleven genotypes were detected comprising 9 high-risk in order of decreasing prevalence HPV-16 (8%), HPV-35 (5%), HPV-33/39/-68 (3%), HPV-52/51/59 (2%) and HPV-18 (1%) and 2 Low-risk types, HPV-42(3%), and HPV-43 (1%). rTh ee women had HPV types that could not be genotyped by our method. Oral contraceptives use was associated with a reduced chance of HPV infection (P=0.002; OR=0.19, 95% CI 0.07-0.54). is Th study found a high HPV prevalence among FSWs in the GAR. A high number of Hr-HPV genotypes seen are vaccine preventable, providing additional compelling argument for implementing a national cervical cancer prevention plan including vaccination. 1. Introduction common female malignancy [3]. In Ghana, it is likely the commonest cancer among women. Current estimates indi- Globally, cervical cancer remains a primary cause of mor- cate that every year 3,151 women are diagnosed with cervical bidity and mortality, with estimated 569,847 new cases and cancer and 2,119 die from the disease in the country [4]. 311,365 attributable deaths in 2018 [1, 2]. The highest incidence Infection of the cervix by a high-risk Human Papillo- has been reported in low and middle income countries, mavirus (HPV), a common sexually transmitted infection, is necessary for the development of cervical cancer [5] particularly in Sub-Saharan Africa where it is the second most 2 Journal of Oncology Many studies have found a direct association of HPV containing DNAgard (Biomatrica, San Diego, CA, USA) for infection with sexual behaviour and have indicated that HPV-DNA detection and genotyping. Samples were collected a high number of lifetime partners may lead to a higher by single use, disposable equipment. transmission of HPV leading to higher cervical cancer rates [6–8]. 2.3. HPV Testing. HPV detection and typing were carried out Female sex workers (FSWs) are a group of females who by Nested multiplex PCR. [10]. A single consensus forward provide sexual services for economic remuneration. Due to primer (GP-E6-3F) and two consensus back primers (GP- exposure to multiple sexual partners in their occupation, E7-5B and GP-E7-6B) were used for HPV DNA detection they are prone to various sexually transmitted infections, in the rfi st round PCR. The PCR reaction mix of 25 𝜇 l including HPV. Sexual contact with FSWs plays an important contained 10X PCR buffer, 2.5mM MgCl 200𝜇 Mofeach role in HPV transmission and might be a major contributor of the four deoxyribonucleoside triphosphates (dNTP’s), to the prevalence of HPV and cervical cancer among women 15pmols of each E6/E7 consensus primers, and 1.25 units in the general population. Also, through the transmission of of Taq polymerase enzyme. Five microliters (5𝜇 l) of DNA the virus to their male clients, they increase the risk of penile extracts was used as a template for the amplification reactions cancers among these men [9]. Furthermore, due to their likely using a thermal cycler (Robocycler Gradient 96, Strategene, interaction with foreign clients and sex tourists, they may USA). The cycling parameters for the rfi st round PCR with possibly havea role in thegenotypediversity of HPV in the E63F/E75B/E76B consensus primers were as follows: 94 Cfor country. four minutes, followed by 40 cycles of 94 C for one minute, ∘ ∘ In Ghana, mortality due to cervical cancer is on the 40 Cfor two minutes, 72 C for two minutes, and a single final rise, most likely due to the lack of an organized preven- elongation step of 72 C for 10 minutes. In the second round tion and control program. Information on circulating HPV PCR, Primers for the identicfi ation of high-risk genotypes 16, genotypes is crucial for determining the impact of cervical 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, and 68 and low-risk cancer control programmes, including HPV immunization. genotypes 6/11, 42, 43, and 44 were used. The primers were The high rates of HPV reported among FSWs make them used in four cocktails, each containing four to vfi e different a priority group for study as we seek to characterize the primer pairs. Two microliters of first round PCR product, 15 prevalent HPV genotypes in the country in order to predict pmols of forward, and reverse primers for genotyping were the likely impact of the current vaccines in reducing the used. The other parameters remained the same as used in incidence of cervical cancer after introduction of mass female the rfi st round PCR. However, the cycling parameters were as ∘ ∘ vaccination in the country. The study also looked at other follows: 94 C for four minutes followed by 35 cycles of 94 C ∘ ∘ factors that may increase the risk of HPV, contribute to for 30 seconds, 56 Cfor 30 seconds, 72 Cfor 45 seconds, and persistence of infection, and/or promote progression of HPV- a single final elongation step of 72 Cfor four minutes [10]. induced changes in the cervical epithelium. Here, we report Positive and negative controls were included in each round the rfi st study of cervical HPV and its associated risk factors of amplicfi ation. among FSW’s in Ghana. The amplicons were resolved on 2% agarose gel stained with 0.5𝜇 g/ml ethidium bromide. Ten microliters of each sample was added to 2𝜇 lof orange G (10X) gel loading dye 2. Methods for the electrophoresis. Hundred base pair DNA molecular 2.1. Study Design and Population. This was a cross-sectional weight marker (Sigma, MO, USA) was run alongside the study undertaken between February and July 2016 in Greater PCR products. The gel was prepared and electrophoresed Accra, one of the ten administrative regions of Ghana in 1X TAE buffer using an electrophoresis tank at 80 volts (and which houses the national capital) with a predomi- for one hour and the gel photographed over an Ultraviolet nantly urban population. A risk factor assessment interview (UV) transilluminator [10]. HPV genotypes were identified was conducted for 100 out of the 109 FSWs who were by comparing the molecular weight of the bands observed to reached through snowballing, to elicit data on their basic positive control band and or the expected amplicon sizes in demographics, sexual activities and behaviours (including each primer cocktail. the age of sexual debut), reproductive history, menarche, sexually transmitted disease (STD) history, screening his- 2.4. Data Analysis. The data obtained through the question- tory, and smoking habit (past and present). Only FSWs naire was checked for accuracy and entered into the computer of age 18 years and above and had been a sex worker for using Microsoft Excel (2016) Programme and was analysed at least 6 months were included in the study. The Ethics using SPSS version 20 (IBM Corp. Armonk, New York, USA). and Protocol Review Committee of School of Biomedical Exploratory analysis was first carried out to obtain descriptive and Allied Health Sciences, University of Ghana, approved statistics. Charts and tables were used to summarize data and this study (SBAHS/10161447/AA/MLS/2015-2016). Partici- display gfi ures where appropriate. The number and propor- pants were fully informed about the purpose, procedures, tion of HPV DNA positives and type-specific HPV infection risks, and benefits of participating in this study and Informed were calculated. To assess the association between HPV DNA consent was obtained from all subjects. positivity and sociodemographic and sexual behavioural factors, odds ratios (ORs) and 95% CIs were calculated using 2.2. Specimen Collection. Following the interviews, a Gynae- logistic regression. In all statistical considerations a p-value cologist collected exfoliated cells from the cervix into tubes <0.05 was considered statistically significance. Journal of Oncology 3 <25 25-34 35-44 45-54 Age group Prevalence Figure 1: Age-specific HPV prevalence. 3. Results 17% (17/100) (Figure 1). Of the HPV positive women, 73.1% (19/26) were infected with only high-risk types, 3.9% (1/26) 3.1. Participant Characteristics. A total of 100 FSW, ages were with only low-risk types, and 11.5% (3/26) had both ranging from 18 to 45 years with a median age of 24 years, high- and low-risk types. were interviewed. More than half (58%) of them were below Table 2 shows the cytological changes found in the high- 25 years. The level of education among the women was risk HPV cases detected with 3 cases each of ASCUS, LSIL, generally low, with the vast majority, 74% (74/100), having and HSIL. at most basic education while 6% (6/100) reported to be illiterates. The median length of sex work was 2 years with 3.3. Risk Factors for HPV Infection. To identify putative risk a range of 0.5-26 years. About a half (53%) of the sex workers factors for HPV infection, we performed univariate regres- reported engaging in other economic activities (mostly petty sion analysis and the results are presented in Table 3. HPV trading) while the rest (47%) were full time sex workers. infection was found not to be significantly associated with, Seventy-seven percent of the subjects who remember their age, education, smoking, average number of clients per week, age at sexual debut recalled it to be≥16 years and 59% of them previous sexual disease, condom use, age at sexual debut, had at least a child. Condom use always was reported by 82% and parity. In contrast, the use of oral contraceptives was (82/100) of the study participants whereas oral contraceptive the only variable that significantly influenced HPV Infection use was reported by 20%. Two (2%) subjects reported to be (P=0.002). Female sex workers who used oral contraceptives HIV positive while 14/100 (14%) had had gonorrhoea, 4/100 had 19% reduced odds of having HPV infection compared to (4%) syphilis, 3/100 (3%) genital warts, and 2/100 (2%) herpes those who did not (OR=0.19, 95% CI 0.07-0.54). before. A third (33%) of them had ever smoked cigarette whist 17% are active smokers. Only 9/100 (9%) had ever undergone 4. Discussion cervical cancer screening. Studies have indicated that a high number of lifetime partners 3.2. HPV Prevalence and Genotypes. The overall HPV preva- may lead to a higher transmission of HPV [6, 7]. The nature lence (any HPV) was 26% (26/100). Eleven genotypes were of work conducted by sex workers predisposes them to an detected comprising 9 high-risk types and 2 low-risk types. increased risk of HPV infection. This study found a crude The high-risk HPV types in order of decreasing preva- HPV prevalence of 26% among female sex workers in the lence were HPV-16 (8%; 8/100), HPV-35 (5%; 5/100), HPV- Greater Region, which is higher than the WHO estimate of 33/39/68 (3%; 3/100), and HPV-51/52/59 (2%; 2/100) HPV- 19.5% HPV Prevalence in women from Western Africa at a 18 (1%;1/100). HPV 42, (3%; 3/100) and HPV-43 (1%; 1/100) given time [3]. This is consistent with existing reports of the were the low-risk HPV types found. In addition 3% (3/100) elevated HPV prevalence in Female sex workers compared had HPV that could not be typed by our method (Table 1). to womeninthegeneralpopulation. Similar studies in There were 21% single HPV infections (including the three other African countries have shown much higher prevalence: that we could not type) and 5% multiple HPV infections. The Madagascar (36.7) among 90 FSWs [11], Senegal (43.5%) 5 multiple infections comprised two each of quadruple- and among 681 FSWs [12], Tunisia (39.2%) among 51 FSWs [13], double-infections and one triple infection. The highest HPV Burkina Faso (66.1%) among 360 FSWs [14], Kenya (55.6%); infection rate was among women aged below 25 years with among 789 FSWs [15], South Africa (62.6%), among 99 HPV Prevalence 4 Journal of Oncology Table 1: Type-specific HPV prevalence. HPV type Single infections Multiple infections Total (%) n=100(100) High-risk infections 16 4 4 8(8) 35 4 1 5(5) 33 2 1 3(3) 39 3 0 3(3) 68 1 2 3(3) 51 2 0 2(2) 52 1 1 2(2) 59 2 0 2(2) 18 0 1 1(1) sub-total 19 10 29(29) Low-risk infections 42 2 1 3(3) 43 0 1 1(1) sub-total 2 2 4(4) Un-typeable X3 0 3(3) Total (LR+HR+X) 24 12 36(36) Table 2: Cytologic changes in HR-positive individuals. (NMPCR) [10] to the conventional PCR (with either MY09- MY11 or GP5+-GP6+ primers) utilized in some of the studies Cytology results HR-Genotypes above, we recorded a lower HPV prevalence compared to NILM 16, 18, 68 those studies. This may likely be due to the fact that 36% NILM 16,35,68 of the FSWs from the Burkina Faso study, 35.2 % from the NILM 33 Kenya study, and 50.3% from the South African study were HIV positive compared to the very low 2% in this study. NILM 39 Cervical HPV infections are substantially more common HSIL 16,33,68 among women infected with HIV, compared with HIV- NILM 52 uninfected women with similar sexual histories due to their NILM 35 impaired immunity and this has been reported by several NILM 16 studies [18–20]. NILM 16 A high number of HPV positive FSWs (17/26), though not NILM 16 statistically significant, were below 25 years. This is consistent NILM 39 with reports in a global review of HPV prevalence among LSIL 16 female sex workers [8]. This observation may be linked with LSIL 35 acquisition of high rates of HPV following commencement ASCUS 51 of sex work. Secondly, this may be related to power play as older sex workers are better able to negotiate condom HSIL 51 use than younger sex workers, although condom use does NILM 35 not provide full protection from HPV infection. This could HSIL 39 also be ascribed to young sex workers enticing more clients ASCUS 16,52 than older sex workers culminating in an increased rate of NILM 35 exposure to HPV. It is however worth stating that more than LSIL 33 half (58%) of our study subjects were within this age bracket NILM 59 and therefore this age trend could have also been due to this ASCUS 59 selection bias. The high-risk HPV genotypes detected in decreasing order of prevalence were 16 (8%), 35 (5%), 33/39/68 (3%), FSWs [16]. These variations could be due to difference in 51/52/59 (2%), and 18 (1%). These genotypes are similar to sampling strategies and HPV assays employed [17] besides what is seen in studies in Ghanaian women with and without cervical cancer and elsewhere in Africa but with vary- risk factors which are known to vary by region. Though we employed a comparatively more sensitive HPV assay ing individual genotype prevalence [21–25]. About 50% of Journal of Oncology 5 Table 3: Results of univariate logistic regression analysis of risk factors for HPV infection. Variables HPV (+) HPV (-) OR (95% CI) P-value Age(years) <25 17 41 0.65 (0.26- 1.67) 0.38 25-34 3 23 3.46 (0.9412.67) 0.06 35-44 6 9 0.46 (0.15-1.46) 0.19 45-54 0 1 - - Education No formal education 1 5 1.81 (0.20-16.27) 0.60 Basic 18 56 1.38 (0.52-3.71) 0.52 Higher 7 13 0.59 (0.20-1.66) 0.31 Time in prostitution (years) <1 6 17 1.45(0.48-4.38) 0.51 1-2 6 27 1.47(0.55-3.94) 0.46 3-4 6 13 0.65(0.21-1.94) 0.44 ≥5 8 15 0.58(0.20-.1.65) 0.31 Full time sex worker Yes 13 34 0.85 (0.35-2.08) 0.72 Average clients per week ≤14 14 40 1.01 (0.41-2.71) 0.99 >14 12 34 1.05 (0.43-2.66) 0.92 Contraceptive Condom 20 62 1.55 (0.52-4.66) 0.44 Oral contraceptive 11 9 0.19(0.07-0.54) 0.002∗ Age at sexual debut(yrs.) <16 7 16 0.74 (0.27-2.09) 0.58 16-20 19 55 1.07 (0.38-2.93) 0.90 >20 0 3 - 0.99 No. of Children 0 11 30 0.93 (0.37-2.30) 0.88 1-2 14 36 0.81 (0.33-1.99) 0.65 ≥3 1 8 3.03 (0.36-25.47) 0.31 Smoking History Current smoking 7 10 0.42 (0.14-1.26) 0.12 Past smoking 9 24 0.91 (0.35-2.32) 0.84 STI in the past Yes 9 14 0.44(0.16-1.11) 0.11 Past STI type Genital warts 1 1 0.34(0.02-5.68) 0.46 Gonorrhoea 5 9 0.58(0.12-5.68) 0.36 Syphilis 2 2 0.33(0.04-2.50) 0.29 Herpes 1 1 0.34(0.02-5.68) 0.46 HIV 2 0 - - high-risk-HPV genotypes detected in this study are covered country even after the institution of a national vaccination by the Nona-valent vaccine (Gardasil 9, Merck) [26] and policy. For example, HPV-35, the second most common therefore the introduction of this vaccine and ultimately a HPV type found in this study, is not a vaccine type. In national vaccination policy would positively impact cervical another study conducted in Ghana among HIV seropositive prevention eor ff ts in the country. However, the fact that not and negative women, HPV-35 was the commonest genotype all high-risk-HPV detected in this and several other studies detected and was significantly associated with Squamous in Ghanaian women with and without cervical cancer are intraepithelial lesions [25]. The low-risk-HPV genotypes vaccine types means cervical screening will continue to play detected, in decreasing order of prevalence, were 42 and 43. an important role in cervical cancer prevention eo ff rts in the These two genotypes were the two common low-risk types 6 Journal of Oncology detected in a study involving pregnant women attending Kwame Wiredu were responsible for design, data generation, antenatal clinic at the Korle-Bu teaching hospital in Accra and data analysis. Abdul Rashid Adams, Richard Harry [23]. Asmah and Edwin Kwame Wiredu took care of manuscript Oral contraceptives use significantly influenced HPV Development. All authors critically reviewed and approved infection (P=0.002), with about 19% decreased chance of the final manuscript. HPV infection in oral contraceptive users compared to nonusers (OR=0.19, 95%CI 0.07-0.54). However, a systematic Acknowledgments review of 19 epidemiological studies of the risk of genital The authors would like to thank all those who agreed to HPV infection and oral contraceptive use concluded that take part in the study, Mr Clement Azigwe, Miss Ramatu, there was no evidence for a strong positive or negative and Sister Janet for their tremendous help in recruiting association between HPV positivity and ever use or long the study subjects. They are grateful to the management duration use of oral contraceptives [27]. There was lack of and staff of All Faith Medical Centre, for allowing their significant association of HPV infection with known risk facility to be used for sample collection and interviews. factorssuchassmoking,ageatsexualdebut,numberofsexual They also deeply appreciate the contributions of Mr. Maxwell partners, and history of STI. These findings could be due Akanburichab, Ms. Kathleen Korkor Glover, Mrs. Lois Botwe, to the small sample size and/or the reliability or otherwise and Mr. Bright Katey of all department of Medical Laboratory of the information provided by the study subjects. The risk science, University of Ghana, during the sample collection factors assessed in this study relied on self-reported data and and interviews. therefore prone to both recall and social appeal bias. Thisisthe rfi st report of cervical HPVand associated References risk factors among FSW’s in Ghana. Our study also has some limitations: this study was done on a small scale; therefore [1] J. Ferlay, M. Ervik, F. Lam et al., Global Cancer Observatory: a larger study with a higher statistical power is needed to Cancer Today, International Agency for Research on Cancer, determine the extent of HPV infection in this population. Lyon, France, 2018. Also, the convenience sampling method employed means the [2] L.Bruni,L. 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