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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 3  |  Issue : 3  |  Page : 170-181

Human papillomavirus associated with head and neck cancer in the Middle East and North Africa: A systematic review and meta-analysis


1 Department of Infection and Immunity, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia
2 Department of Sexually Transmitted Infections, National Public Health Laboratory, Saudi Center for Diseases Prevention and Control, Riyadh, Saudi Arabia
3 College of Medicine, Alfaisal University, Riyadh, Saudi Arabia

Date of Submission18-Dec-2019
Date of Decision19-Jan-2020
Date of Acceptance21-Jan-2020
Date of Web Publication02-Jul-2020

Correspondence Address:
Fatimah Saeed Alhamlan
MBC 03, P.O Box 3354, Riyadh 11211
Saudi Arabia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/JNSM.JNSM_70_19

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  Abstract 


Background: Head and neck cancer (HNC) is associated with tobacco or heavy alcohol use and chronic human papillomavirus (HPV) infection. Aims and Objectives: In this systematic review and meta-analysis, we determined the HPV-associated HNC prevalence rates and potential factors affecting prevalence rates in the Middle East and North Africa (MENA) region. Materials and Methods: Between July and August 2019, we searched and collected 38 articles from PubMed and Medline databases related to head and neck squamous cell carcinoma and HPV in the MENA region. Of those articles, 25 met the inclusion criteria. Results: The overall pooled HPV prevalence rate of all HNC cases reported in the MENA region was 16% (confidence interval 95%, 12%–21%). HPV was found primarily in the salivary glands (20%) and tonsils (16%). The characteristics of patients associated with HPV-driven HNC were being male, having a benign tumor, and using tobacco. The genotypes most strongly associated with HNC in the MENA region were HPV-16 followed by HPV-18. The highest reported prevalence rates of HPV-associated HNC were in Turkey (48%) and Palestine-Israel (31%), whereas the lowest were in Yemen (2%) and Saudi Arabia (4%). HNC-associated HPV prevalence decreased over time in the MENA region, from 19% during 1998–2010 to 15% during 2011–2014 to 12% during 2015–2019. Conclusion: Although the current prevalence of HPV-associated HNC in this region is low relative to rates observed elsewhere, HNC is typically fatal, and a global rise in HPV-driven HNC indicates that additional studies should be conducted in the MENA region to address this risk and to develop HPV awareness, screening, and vaccination programs.

Keywords: Head and neck cancer, human papillomaviruses, Middle East and North African region, oral cancer


How to cite this article:
Asiri SS, Obeid DA, Alhamlan FS. Human papillomavirus associated with head and neck cancer in the Middle East and North Africa: A systematic review and meta-analysis. J Nat Sci Med 2020;3:170-81

How to cite this URL:
Asiri SS, Obeid DA, Alhamlan FS. Human papillomavirus associated with head and neck cancer in the Middle East and North Africa: A systematic review and meta-analysis. J Nat Sci Med [serial online] 2020 [cited 2020 Aug 15];3:170-81. Available from: http://www.jnsmonline.org/text.asp?2020/3/3/170/288829




  Introduction Top


Worldwide, 650,000 new cases of head and neck cancer (HNC) are detected every year, accounting for 330,000 deaths annually.[1] The major high-risk factors for HNC include tobacco use, alcohol consumption, and viral infections, such as human papillomavirus (HPV) or Epstein–Barr virus.[2] In many developed countries, the number of HNC cases related to tobacco use have been declining; however, the number of oropharyngeal cancer (OPC) cases are increasing.[3] Numerous studies attribute the rise in number of OPC cases to increased numbers of HPV cases and a change in sex behavior norms.

HPV is an oncogenic virus that is strongly associated with several cancers, including cervical, anal, oropharynx, penile, vaginal, and vulvar cancers. The incidence rate of HPV-related HNC is close to 7%, which is notably lower than that reported for cervical cancer.[4] HNC mostly presents in male patients, with many studies reporting a prevalence of 69% of the HNC cases to be for male patients.[5] The main subtypes of HNC are oral squamous cell carcinoma (OSCC) and oropharyngeal squamous cell carcinoma. Several studies have reported that in women, the prevalence rate of oral HPV is 2%–3%, whereas the cervical HPV prevalence rate is 81% and the anal HPV prevalence rate is 43%.[6],[7] Other studies have reported that HPV has been detected in oral dental settings at 5.5% of the general population.[8] Overall, the rate of HPV-related HNC incidence is low. However, owing to the poor prognosis of HNC and the availability of preventable measures against HPV, more studies need to address the increasing trend in HPV-driven HNC. Preventable measures against chronic HPV infection include using condoms, participating in systematic screening, and vaccinating against HPV (especially high-risk types 16 and 18). The most detected genotype of HPV in HNC is the high-risk type HPV-16, accounting for approximately 80% of the cases.[9],[10] Sex behaviors such as oral sex or multiple partners or men who have sex with men increase the risk of HNC.[11]

In the Middle East and North Africa (MENA) region, studies investigating the HPV incidence rate in HNC patients are scarce. People in the MENA region share similar conservative cultural values and behaviors. However, one study conducted using the GLOBOCAN 2012 statistics estimates that the risk of HNC will double in 2030 in the MENA countries of Egypt, Iran, Morocco, Sudan, and Turkey.[12] This increase may be attributable to the high tobacco use in those countries. However, the role of HPV in the suggested increase in the MENA region needs to be thoroughly investigated and addressed. Most of the countries in the MENA region have no HPV prevention measures in place, such as screening or vaccination programs. One exception is Libya, which has an active vaccination program in some regions. However, the challenges of coverage and high cost remain throughout most of the MENA region.

The aim of this systematic review and meta-analysis was to report the prevalence of HPV in HNC stratified by clinical and demographic groups in the MENA region. Other objectives of our study are to investigate potential factors affecting the incidence of HPV, to study the general distribution of HPV genotypes by MENA region, and to estimate the importance of HPV testing in the MENA region and its association with HNC cases.


  Methods Top


Data sources and search strategy

This study followed the Preferred Reporting Items for Systematic Reviews and Meta-analyses reporting guideline.[13] The search was conducted between July and August 2019; the articles were downloaded into the reference manager. PubMed and Google Scholar databases were searched using the keywords “HPV,” “HPV,” “oral cancer,” “head and neck cancer,” “oropharynx cancer,” “OPC,” “OSCC,” and “HNSCC.” The search criteria for the MENA region countries included Algeria, Bahrain, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Palestine-Israel, Qatar, Saudi Arabia, Sudan, Syria, Tunisia, the United Arab Emirates, and Yemen. The search strategy was designed to capture as many studies as possible that meet the eligibility criteria, ensuring that relevant time periods and sources are covered and not restricted by language or publication status.

Study selection and inclusion and exclusion criteria

The search results were imported into the Mendeley reference manager and screened for duplicates. The abstracts of the unduplicated articles were then screened manually. The inclusion criteria included the reporting of the prevalence of HPV as determined using standardized diagnostic assays in any of the MENA region countries. The exclusion criteria included case reports, reviews, editorials, letters to editors, commentaries, animal studies, and seroprevalence studies.

Data extraction and validity assessment

The data extracted from each study to be used in the present meta-analysis were the first author's surname, type of HPV screening, sample size, year of publication, country and city of origin, anatomic site of cancer, type of cancer, sex (if reported), tobacco use (if reported), and most common HPV genotype. Each study was validated and checked by two reviewers, and in case of dispute, a third reviewer was assigned.

Statistical analysis

The meta-analysis was conducted using the software program MetaXL EpiGear, version 5.3 (Sunrise Beach, Queensland, Australia) and the SAS statistical package, version 9.4 (Cary, NC, USA) the Statistical Package for the Social Sciences (SPSS), version 25 (Chicago, IL, USA), was used to generate the figures. Pooled prevalence estimates were calculated using the DerSimonian and Laird method, a random-effects meta-regression model.[14] The Cochran Q and I2 statistics were calculated to assess the study heterogeneity. The Chi-squared test was used to assess heterogeneity, and tau-squared (τ2) was calculated to assess the variability in the variance between the studies. The pooled prevalence and the corresponding 95% confidence intervals (95% CIs) were used to compare the HPV prevalence rates between different factors. The Mann–Whitney test was conducted between head and neck squamous cell carcinoma (HNSCC) and OSCC groups to determine whether the prevalence of the HPV rates was significantly different. Analysis of variance (ANOVA) tests were also conducted to assess whether any of the factors (anatomic site of cancer, country, and HPV type) affected the prevalence rates of HPV in the sample population. A two-sided P < 0.05 was identified as a statistically significant difference.


  Results Top


Characteristics of included studies

The study selection diagram is shown in [Appendix 1] - [Figure 1]. The primary search found 24 published studies, and the additional search located 14 published studies. After reviewing the collected published studies, five studies were removed, due to their irrelevance, detection assays, and countries that were included in the study and one was found to be duplicated. Overall, for the meta-analysis, 25 published studies met the inclusion criteria and were used, and subgroups were created from the clinical and demographic data. The main clinical populations were subdivided into HNSCC, which included all head and neck anatomical sites except for oral sites, and OSCC, which comprised all the oral sites, including oral mucosa, tongue, the anterior floor of the mouth, posterior mandibular region, the soft palate, and the labial mucosa.



Human papillomavirus prevalence in the Middle East and North Africa region by clinical and demographic data

On the basis of the 25 published studies examined in the present meta-analysis, the pooled HPV prevalence rate was 16% (95% CI, 12%–21%). A high heterogeneity rate (89%) between the studies collected was found. For the patient groups, the studies indicated that patients with HNSCC had a higher pooled prevalence (19%) than those with OSCC (13%). However, this difference was tested using the Mann–Whitney test and was not statistically significant (P = 0.124) [Appendix 2] - [Table 1]. [Figure 1] and [Figure 2] show the distribution of HPV across the different studies using forest plots. For both HNSCC [Figure 1] and OSCC [Figure 2], most studies reported prevalence rates higher than the pooled prevalence rates.
Table 1: Pooled human papillomavirus prevalence by clinical data in the Middle East and North Africa region and heterogeneity measures among studies

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Figure 1: The pooled prevalence of human papillomavirus cases related to the head and neck squamous cell carcinoma population in the Middle East and North Africa region. The DerSimonian and Laird random-effects meta-regression model was used for the meta-analysis of studies included in the head and neck squamous cell carcinoma population in the Middle East regions. The pooled human papillomavirus prevalence was 19% (n = 880) and is represented by the middle of the solid diamond. The width of the solid diamond represents the pooled means. Squares represent mean values, with error bars representing 95% confidence intervals

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Figure 2: The pooled prevalence of human papillomavirus cases related to oral squamous cell carcinoma population in the Middle East and North Africa region. The DerSimonian and Laird random-effects meta-regression model was used for the meta-analysis studies included in the oral squamous cell carcinoma population in the Middle East region. The pooled human papillomavirus prevalence was 13% (n = 1388) and is represented by the middle of the solid diamond. The width of the solid diamond represents the pooled means. Squares represent mean values, with error bars representing 95% confidence intervals

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For the anatomic regions where cancer metastasized, the prevalence of HPV was reported to be highest in salivary glands (20%) and tonsils (25%). By contrast, the lowest reported prevalence rates of HPV by anatomic region were in multiple metastasized regions (6%) and in oral regions (16%). Overall, higher HPV prevalence rates were reported in male patients, who have benign tumors, and tobacco users. The summary of the pooled prevalence rates and the clinical data by heterogeneity measures is given in [Table 1]. The distribution of HPV by anatomic region is shown in [Figure 3].
Figure 3: Distribution of human papillomavirus prevalence reported without normalization in multiple studies by anatomic site. The prevalence rate is the highest in the oral cavity, followed by the salivary glands and pharynx. The prevalence of human papillomavirus is lowest in patients with multiple infected regions. The horizontal band in each bar represents the maximum value; the ends of the bars is the lowest value; and the error bars are 95% confidence intervals

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The specific anatomic regions where cancer was reported to metastasize in all of the reviewed studies are given in [Table 2]. The highest number of HPV cases was detected in the oral cavity. An ANOVA was conducted comparing the effect of anatomic region on HPV prevalence rates, and the results are given in the [Appendix 2] - [Table 2] and [Table 3]; however, no statistical difference was detected, suggesting that tumor site has no effect on HPV prevalence rate.
Table 2: Human papillomavirus pooled prevalence rate by anatomic region and the number of studies that reported detecting human papillomavirus at that site

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Table 3: Pooled human papillomavirus prevalence in the Middle East and North Africa region and heterogeneity measures among studies

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The summary of the geographic data and HPV prevalence rates are given in [Table 3]. The pooled prevalence rates were similar (14%) in the regions of Turkey-east Asia and North Africa. The highest reported prevalence was detected in Turkey (48%) and in Palestine-Israel (31%). The lowest prevalence rates were detected in Yemen (2%) and Saudi Arabia (4%). [Figure 4] shows the distribution of HPV by country and clinical group. For OSCC, the highest prevalence was reported in Egypt, followed by Sudan, Iran, Saudi Arabia, and Yemen. For HNSCC, the highest prevalence rate was reported in Palestine-Israel, followed by Iran, Saudi Arabia, and Sudan.
Figure 4: Distribution of human papillomavirus prevalence by clinical group and country. For head and neck squamous cell carcinoma cases, the highest reported prevalence was in Iran, followed by Egypt. For oral squamous cell carcinoma, the highest reported cases were in Egypt followed by Sudan. The horizontal band in each bar represents the maximum value; the ends of the bars are the lowest value; and the error bars are 95% confidence intervals. Countries with single value are represented by dash, and the asterisk represents suspected outlier

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Human papillomavirus prevalence in the Middle East and North Africa region by year of conducted surveillance

The meta-analysis showed an overall pattern of decreased HPV prevalence over the years. [Figure 5]a shows the distribution of HPV by year and indicates that only a few studies on HPV prevalence were reported before 2005. Many studies reported low HPV prevalence rates, especially after 2010. [Figure 5]b shows the summary statistics of the pooled prevalence rates and the study statistics. Higher prevalence rates were reported in earlier years, whereas most of the recent studies have reported a lower prevalence rate.
Figure 5: The effect of time on the prevalence of human papillomavirus reported in the Middle East and North Africa region. (a) Distribution of human papillomavirus prevalence by year of article publication. Human papillomavirus prevalence rate has decreased over the years. (b) Summary of the pooled human papillomavirus prevalence by year group. The highest prevalence rates were reported in studies conducted in between 1998 and 2010, whereas the lowest prevalence rates are reported in later years (2015-present)

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Human papillomavirus genotypes detected in head and neck squamous cell carcinoma and oral squamous cell carcinoma in the Middle East and North Africa region

Most of the studies analyzed did not report HPV genotyping results. However, those that did showed that the most detected type in HNSCC and OSCC was HPV-16 followed by HPV-18. HPV-16 was primarily detected in the oral cavity, followed by the pharynx; similar results were also found for HPV-18. [Figure 6] shows the distribution of HPV genotypes in the MENA region by anatomic site. HPV-16 infection was mostly associated in multiple anatomical regions, while HPV-18 was mostly reported in the pharynx and oral cavity.
Figure 6: The most commonly detected human papillomavirus genotype among patients with oral head and neck squamous cell carcinoma in the Middle East and North Africa region. The most detected Genotype in most of the studies is human papillomavirus-16, followed by human papillomavirus-18

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[Figure 6] show the most commonly detected HPV genotype among patients was OSCC and HNC in the MENA region. The most detected genotypes in the MENA region are HPV-16 which is found multiple anatomical regions, followed by HPV-18 which is mostly detected in the pharynx and oral cavity.

Regression analysis examining the effects of clinical and demographic factors on human papillomavirus prevalence rates

The use of univariate and multiple regression models to estimate HPV prevalence rates showed no statistically significant effect of clinical or demographic factors. As shown in [Appendix 3] - [Table 1], [Table 2], [Table 3], none of the multiple regression models were significant, and the overall ANOVA for each model was also not significant. However, the estimated CIs for the pooled HPV prevalence using multiple models with all factors [Appendix 3 - [Table 1] were significant for Iran, Egypt, Turkey, Palestine-Israel, and Lebanon. For the second model, which comprised all factors except the HPV types, the model showed a lower significance, and only Iran, Egypt, and Turkey had a significant association with prevalence rates. For the third model [Appendix 3 - [Table 3], which consisted of only the clinical groups (HNSCC and OSCC) and anatomic region, the predicted intervals were significant for the clinical groups, with a lower risk for the HNSCC group compared with the OSCC group.



In the univariate models, none of the independent models could predict HPV prevalence on their own [Appendix 3] -[Table 4] and [Table 5]. For the clinical group, the model indicated significant CIs, with the HNSCC group showing lower intervals (1%–55%) than the OSCC group. For the second independent model, the anatomic sites were examined, and none of the intervals were able to predict HPV prevalence.{Table 4}{Table 5}


  Discussion Top


We conducted a systematic review and meta-analysis study to determine the current burden of HPV cases associated with HNC in the MENA region. We were successful in determining the prevalence of HPV-associated HNC cases, and we also determined the clinical and demographic factors associated with the HPV-associated HNC cases.

Our meta-analysis estimated an overall prevalence of HPV in HNC cases of 16% from 25 studies with a population size of 2342 cases. More specifically, patients in the HNSCC group had a higher prevalence rate of HPV (19%) than those with OSCC (13%). Other global studies have similarly reported a higher incident rate of HPV in patients with HNSCC patients (approximately 33%) compared with patients with OSCC (approximately 27%).[15] Overall, the rate of HPV prevalence for both cancer groups calculated in our meta-analysis was significantly lower than that reported in some individual studies. A few studies have reported that the rate of HPV infection has been increasing over the years; however, this trend was observed mainly in North America and Europe.[16],[17] By contrast, we found that the prevalence of HPV has been decreasing with time in the MENA region. However, this trend could not be fully evaluated in the present study because most of the included studies were published in the late 2000s. This shortcoming is the result of an insufficient number of peer-reviewed articles evaluating HPV-associated HNC cases in the MENA region. The present meta-analysis also evaluated potential factors associated with a higher risk of HNC, including sex, etiological site, and smoking status. By sex, male patients with HNC were more likely to have HPV infection than female patients. This observation is consistent with other studies.[18],[19] For the etiological site, our meta-analysis indicated that the most common sites where HPV manifests in HNC cases were in the tonsils and salivary glands. Other reviews have reported a similar association of HPV with higher prevalence in the tonsil region.[20] We found that the lowest reported prevalence of HPV by etiological site was in oral regions (16%).

Smoking is strongly linked with cancer. For HNC, the risk for smokers is almost 10-fold more than that for nonsmokers. This risk has been well reported, with the strongest association being that for OPC.[21] Many countries, including the United States, have significantly decreased the number of tobacco users; however, the number of HNC cases remain high. Researchers have attributed this to an increase in HPV infections.[22] Smoking among people in the MENA region is higher than that among people in the United States and slightly higher than that among European countries, but it is lower than that among individuals in Asia. In a survey study conducted in the MENA region, the prevalence of smoking was highest in the Levant region and Turkey, followed by Egypt and the Gulf countries, whereas the lowest rate of smoking was reported in Morocco.[23] For HPV prevalence rates related to HNC cases, Turkey and the Levant region also reported the highest prevalence of HPV-associated HNC cases; however, the lowest rates were reported in Yemen and Saudi Arabia.

By geographic site, the highest prevalence of HPV-associated HNC cases was in Turkey (48%) and Palestine-Israel (31%), whereas Saudi Arabia had the lowest prevalence. However, by region, both North African and East Asian countries in the Middle East have a prevalence of 14%. In Europe, where many countries have implemented HPV vaccination programs, the HPV prevalence in HNC cases is approximately 40%, with the highest prevalence by anatomic region of HPV in the tonsils (66%) and the lowest in the tongue (26%).[24] One article from Africa reports a prevalence of HPV associated with HNSCC cases to be 18%, which is closer to what we detected in the MENA region.[25] China has an HPV-16–associated HNC prevalence of approximately 25%, which is higher than that detected in most of the MENA region.[26] Overall, the trend of HPV infection prevalence rates by region in our meta-analysis was closer to those observed in Africa, followed by Europe.

For HPV genotype, we reported a high HPV-16 prevalence in HNC cases found in multiple anatomic sites, whereas HPV-18 associated with HNC cases was primarily located in the pharynx and the oral cavity. Other studies have reported a high prevalence of HPV-16 associated with OPC, while HPV-18 is mostly detected in the larynx.[27]

A main challenge for people with HPV-driven HNC is the variability of treatment options because of the complications associated with this type of HNC compared with treatment for people with HNC that is genetically driven. One study reports that HPV-driven HNC cases are mostly associated with P16, and patients are less likely to harbor the P53 mutation; thus, treatment of these patients is highly variable.[28] Because treatment of HPV-driven HNC needs to be personalized, new biomarkers are needed, and a line of targeted therapy needs to be developed and tested.


  Conclusion Top


This systematic review and meta-analysis determined the current prevalence rates of HPV associated with HNC in the MENA region. Although many countries in this region have a low HPV prevalence rate, others, such as Turkey and Palestine, still face a higher threat. Vaccination programs should be considered throughout the region because the rate of HPV infection is still increasing globally. Many countries in the MENA region lack vaccination and awareness programs, and thus efforts aimed at increasing these programs and awareness are needed to help control HPV and decrease its associated cancers.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

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