Epidemiological patterns of cervical human papillomavirus infection among women presenting for cervical cancer screening in North-Eastern Nigeria

This study reveals a 48.1 % prevalence of cervical HPV infection among women who presented for cervical cancer screening in Gombe, north-eastern Nigeria. It is one of the highest prevalence rates among one of the oldest studied populations (mean age of 39.6 ± 10.4 years) to be ever reported from any part of Nigeria and the first from North-Eastern Nigeria [6, 10, 11, 18–20]. Although there are only a few studies from Northern Nigeria, a high prevalence of 76 % reported from Kano further highlights the possibility of this region carrying the highest HPV burden in the country [18].

Several Nigerian studies among diverse population groups had reported lower prevalence rates including 19.6 % among HIV infected patients in Lagos [19], 26.3 % in Ibadan [11], 14.7 % in Irun [6] and 25 % in Abuja [21]. This disparity may be explained by variations among the different study populations with varying exposures to different risk factors based on diverse socio-cultural and geographical differences. This study was conducted among women presenting for cervical cancer screening with many of them being referred by a healthcare worker following complaints of symptoms suggestive of either genital tract infection or cervical cancer. Hence, they are naturally a selected “high risk” group for HPV infection. There is widespread polygamy and early marriage [13], with cervical cancer being the commonest genital tract malignancy in this poorest region of the country [12, 14]. Early pregnancy and high parity are all very common in North-Eastern Nigeria [22]. These and probably other unreported risk factors in the locality could be responsible for the high prevalence of HPV infection in this “high risk region”.

Studies done in other parts of sub-Saharan Africa among similar population groups have shown similarly high prevalence rates when compared to the value in this study. A prevalence of 66.1 % had been reported among high risk women in Burkina faso [23] while 49.6 % and 60.7 % were also reported among women in Kenya and Sudan respectively [24, 25]. In contrast, some non-African countries showed lower prevalence even among similar population groups with 5.5 % in Iran [26], and 23.6 % in China [27]. This has further buttressed the fact that sub-Saharan Africa, particularly Nigeria carries one of the highest burden of HPV infection in the world [7, 11]. The predominance of most positive risk factors for HPV alongside inadequate knowledge and awareness about this virus in Africa could be an explanation for the higher prevalence of the infection in this continent. Moreover, from evolutionary point of view, there are predictions that the root of some if not all HPV types could be traced to Africa [28].

The predominance of HPV types 16 and 18 as observed in this study follows the global trend and is in conformity with some Nigerian studies [11, 18]. However, the observed predominance of HPV 18 as against type 16 in this study is in concert with a similar study from Kano in Northern Nigeria [18]. This suggests the possibility of Northern Nigeria harbouring a higher prevalence of HPV 18 than 16 in contrast to the general global trend. Although very few studies are available to justify this assertion, geographical differences associated with HPV type distribution had been previously reported from other parts of the world [29]. Variations were particularly observed in predominance between the other HPV types found in this study in comparison to most other Nigerian studies from southern part of the country [10, 11, 19]. The predominant HPV types were also different from those reported in Abuja (North-central Nigeria) [21]. This may be attributable to geographical variations in addition to culture and other life styles or partly because most of the studies restricted their search to specific HPV types while this study had the advantage of using DNA sequencing to detect wider variety.

Seven (HPV types 16, 18, 31, 33, 35, 45 & 58) out of the eight (HPV types 16, 18, 31, 33, 35, 45, 52 and 58) global most common cervical HPV types among women were also found in this study [30]. The five HPV types (16, 18, 31, 33 and 45) responsible for 80 % of cancers [31] are also about the most predominant in this study accounting for 13.2 %, 44.7 %, 5.3 %, 7.9 % and 2.6 % for HPVs 16, 18, 31, 33 and 45 respectively. This may probably have contributed to the higher prevalence of cervical cancer in Northern Nigeria [14]. HPV- KC5 has been reported to be present in the normal skin among some rural dwellers in China [32]. More recently, it was also found in the respiratory tract suggesting the possibility of its presence in some other parts of the body [33]. HPV-KC5 may not confer a risk for cervical cancer as it does not belong to alpha HPV species which contain all the types responsible for cervical cancer [3].

Low prevalence of multiple HPV infections as observed in this study compared to studies that used type specific primers (TS-PCR) in genotyping is not unusual [18]. Sequencing has however been shown to detect more genotypes than TS-PCR suggesting the need to combine both methods for maximum yield [34]. This study utilized nested PCR using PGMY 09/11 and GP5+/GP6+ which has been shown to be sensitive in detecting wider range of HPV genotypes and also relatively more effective in detecting multiple infections[35]. However, the inability of this study to detect low risk HPV genotypes may be attributable the PGMY 09/11 primer which has low capacity of detecting lr-HPV and the fact they are generally fewer in cervical specimens and also more common among males than females [35–37].

Several variables (level of education, age at sexual debut, age at first pregnancy, parity, lifetime sexual partners and history of other malignancies) observed in this study revealed a statistically significant association with HPV infection. Low socio-economic status, early marriage/coitarche, polygamy and high parity are all well-established risk factors for HPV infection [7, 38]. Women with lower levels of education were found to have a higher risk of HPV infection as shown in this study and another Nigerian study [21]. Higher educational level among women is generally associated with increased knowledge/attitude towards HPV and its preventive measures with minimal risk factors for the infection[39]. This has also been observed in this study as many of participants were highly educated up to tertiary level as against the corresponding 2 % among the general female population in the area[12]. Therefore, this study may not depict the true picture of the general population. A study among cervical cancer screening population group in Lagos, Nigeria also reaffirmed the statistical significance of age at sexual debut, parity and lifetime sexual partners as risk factors for HPV infection [20]. In contrast to this study, Adegbesan-Omilabu et al., and Rocha-Brischiliari et al. all reported the use of oral contraceptive pills, HIV infection and cigarette smoking as significant risk factors for HPV infection [2, 40]. This may be attributed to the relatively few percentage of women that responded to questions on smoking history (0.5 %), use of hormonal contraception (44.5 %) and HIV infection (5.2 %). Possible variations in the duration of exposure to these factors among different studied populations may also be contributory. Women with longer duration of exposure to oral contraceptives have been shown to have 2-fold increase in risk of acquiring HPV infection [41]. In concert with this study, marital status, presence of co-wives, religion and tribe were all not statistically significant risk factors for HPV as highlighted by some Nigerian studies [20]. Also unrelated to the risk of HPV infection in this study is the use of condom as has also been observed in Ibadan by Thomas et al. [10].

Majority of the studied population fell within the age group 30 to 45 years, hence are suitable for enrolment in screening and treatment programmes in preventing cervical cancer [6]. In addition, up to 166 (79.8 %) of the participants in this study were above 30 years of age which shows that majority may be having a persistent HPV infection (the actual risk for developing cervical cancer). This finding further reaffirms the suitability of HPV DNA detection as an important diagnostic tool for cervical cancer screening in this population [42].

Logistic regression analysis of the identified risk factors showed that university education, multiple sexual partners, multiparity and grand multiparity are associated with a significantly increased likelihood of having HPV infection among the participants. The apparent significance of university education as a risk factor against our earlier observation and the general trend may not be unconnected with skewed distribution of the respondents in terms of educational qualification. These findings further confirm the need for a larger and community based study to obviate the lopsided distribution of the participants as majority of them are educated and screening is mostly based on referral by healthcare workers.

HPV Prevalence of 48.1 % was recorded from this study. Eleven different HPV types were detected with the five most predominant types (sequentially) being 18, 16, 33, 31 and 35. Other types were 38, 45, 56, 58, 82 and KC5. Low level of education, early age at sexual debut, high parity, multiple life time sexual partners, early age at first pregnancy and positive history of other malignancies were the significant risk factors associated with cervical HPV infection in Gombe.

This study has revealed north-eastern Nigeria as having one of the highest HPV prevalence in the country and also a region that will benefit from the currently available HPV vaccines.

There is need for a universal, well-coordinated, multi-centred, rural and urban community based study on HPV in addition to a comprehensive national cervical cancer screening programme and improved availability/accessibility of the currently available HPV vaccines in all parts of Nigeria.