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Prognostic Significance of HPV and P16 Status in Men Diagnosed with Penile Cancer: a Systematic Review and Meta-Analysis

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Published OnlineFirst July 9, 2018; DOI: 10.1158/1055-9965.EPI-18-0322 Review Cancer Epidemiology, Biomarkers Prognostic Significance of HPV and p16 Status in & Prevention Men Diagnosed with Penile Cancer: A Systematic Review and Meta-analysis Freja Lærke Sand1, Christina Louise Rasmussen1, Marie Hoffmann Frederiksen2, Klaus Kaae Andersen2, and Susanne K. Kjaer1,3 Abstract It has been shown that human papillomavirus (HPV) of DSS, we included 649 men with penile cancer tested for and p16 status has prognostic value in some HPV-associ- HPV (27% were HPV-positive) and 404 men tested for p16 ated cancers. However, studies examining survival in men expression (47% were p16-positive). The pooled HRHPV of with penile cancer according to HPV or p16 status are often DSS was 0.61 [95% confidence interval (CI), 0.38–0.98], inconclusive, mainly because of small study populations. andthepooledHRp16 of DSS was 0.45 (95% CI, 0.30– The aim of this systematic review and meta-analysis was to 0.69). In conclusion, men with HPV or p16-positive penile examine the association between HPV DNA and p16 status cancer have a significantly more favorable DSS compared and survival in men diagnosed with penile cancer. Multi- with men with HPV or p16-negative penile cancer. These ple electronic databases were searched. Twenty studies findings point to the possible clinical value of HPV and were ultimately included and study-specific and pooled p16 testing when planning the most optimal management HRs of overall survival and disease-specific survival (DSS) and follow-up strategy. Cancer Epidemiol Biomarkers Prev; 27(10); 1– were calculated using a fixed effects model. In the analysis 10. Ó2018 AACR. Introduction negative vulvar cancer (12). Penile cancer displays many similar- ities to vulvar cancer including histology, risk factors, and natural Penile cancer is a relatively rare malignancy with approximately history (13); however, studies examining the association between 26,000 new cases diagnosed each year globally (1). The incidence HPV status and survival in penile cancer are often inconclusive of penile cancer varies among different geographic areas, being because of small study populations. Knowledge on possible highest in less developed countries (2). Two major etiologic differences in prognosis of HPV-positive and -negative penile pathways of penile carcinogenesis have been suggested; one cancers could be of clinical interest as it might provide insight involves high-risk human papillomavirus (HPV), which is into the clinical outcome of the patients, guide treatment deci- detected in nearly 50% of penile cancers, with HPV16 being the sions and subsequent follow-up strategy. most prevalent genotype (3, 4). The other pathway involves In addition to HPV, the immunohistochemical (IHC) marker, nonviral mechanisms where the cancers often develop on the p16, is of potential interest in the prediction of prognosis fol- background of the inflammatory skin condition lichen sclerosus lowing a cancer diagnosis. Integration of high-risk HPV DNA into (5–7). the host genome causes overexpression of E7 and E6 oncopro- HPV status has been identified as a possible prognostic marker teins. E7 binds to hypo-phosphorylated retinoblastoma protein, in some HPV-associated cancers; specifically, HPV-positive oro- which leads to overexpression of the tumor suppressor protein, pharyngeal squamous cell carcinomas (SCC) have a more favor- p16. Overexpression of p16 can be detected by, for example, IHC able clinical outcome compared with HPV-negative (8–11). In staining and serves as a reliable marker for the presence of high- addition, in a recent meta-analysis we found that women with risk HPV infection (14). Furthermore, it has been suggested that HPV-positive vulvar cancer have a superior overall survival (OS) p16 might be a strong independent prognostic marker in oro- and disease-free survival (DFS) compared with women with HPV- pharyngeal SCC (15, 16). The aim of this study was to examine the association between HPV DNA and p16 status with survival in men diagnosed with 1Unit of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark. 2Unit of Statistics and Pharmacoepidemiology, Danish penile cancer. In this review and meta-analysis, we systematically Cancer Society Research Center, Copenhagen, Denmark. 3Department of Gyne- searched different databases to identify relevant literature to cology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark. calculate pooled HRs of different survival outcomes comparing Note: Supplementary data for this article are available at Cancer Epidemiology, HPV DNA-positive or p16-positive penile cancers with the respec- Biomarkers & Prevention Online (http://cebp.aacrjournals.org/). tive negative ones. Corresponding Author: Susanne K. Kjaer, Danish Cancer Society Research Center, Copenhagen, DK-2100, Denmark. Phone: 4535257663; E-mail: Materials and Methods [email protected] Search strategy and eligibility criteria doi: 10.1158/1055-9965.EPI-18-0322 We performed a systematic literature search in the electronic Ó2018 American Association for Cancer Research. databases PubMed, Embase, and Cochrane Library up to July 20, www.aacrjournals.org OF1 Downloaded from cebp.aacrjournals.org on September 27, 2021. © 2018 American Association for Cancer Research. Published OnlineFirst July 9, 2018; DOI: 10.1158/1055-9965.EPI-18-0322 Sand et al. 2017. We used combinations of search terms (structured vocab- model to pool the data weighing the studies according to size and ulary and free text) for penile cancer, HPV, p16, and survival. The significance of results, according to the method described (19). search was restricted to English language publications. In addi- Statistical heterogeneity across studies was evaluated by the I2 tion, the reference lists of included studies were reviewed to statistics, which describes the percentage of total variation that is identify other relevant publications. Studies reporting survival caused by heterogeneity rather than chance (22). Significance of outcome after histologically verified penile cancer in relation to the heterogeneity was determined by Cochran's Q test and a HPV or p16 status in five or more cases were eligible for inclusion. P-value <0.05 was considered significant (22, 23). All analyses Only peer-reviewed studies were included. If a study population were conducted using the statistical software R (24), with the was described in more than one paper, only data from the paper package "meta" (25). with the most complete information was used. The study was conducted in accordance with "preferred report- ing items for systematic reviews and meta-analyses" (PRISMA) Results guidelines (17). Search results We identified 616 records in the electronic databases (PubMed, Quality assessment Embase, Cochrane; Fig. 1). Initially, we excluded duplicates (n ¼ The quality of the included studies were assessed according to a 167), leaving 449 titles to be screened for potential relevance. critical review checklist that the Meta-analysis Of Observational Based on review of titles we excluded 352 records, and 54 records Studies in Epidemiology (MOOSE) group of the Dutch Cochrane were excluded after evaluation of the abstract. From the remaining Center has proposed (18). The following information was eval- 43 studies, 23 were excluded based on review of the full text. The uated in each study: study design, study population (e.g., number reasons for exclusion of records are specified in Fig. 1. In total, 20 of cases, type of histology, stage and grade of the tumors, age of the studies were included in the review and meta-analysis. Two study population and treatment), assessment of reported out- studies (26, 27) had overlapping study populations, but reported comes, period of follow-up, and methods applied for respectively different survival outcomes and were therefore both included. HPV DNA and p16 testing. No studies were excluded based on the quality assessment. Study characteristics The characteristics of the included studies (n ¼ 20) are pre- Data extraction sented in Table 1. The studies were published between 1992 and Two authors (F.L. Sand and C.L. Rasmussen) independently 2017. The majority of the studies originated from Europe (n ¼ 9; reviewed titles, abstracts, and full-text articles, and conducted the refs. 20, 28–35) and United States (n ¼ 6; refs. 21, 36–40). The data extraction. Any inconsistencies in the selection of relevant remaining studies came from Brazil (n ¼ 4; refs. 26, 27, 41, 42) papers or the data extraction were discussed to reach consensus. and Canada (n ¼ 1; ref. 43). The median or mean age of the men Data tables were made to systematically extract all relevant data with penile cancer was mostly in mid 60s ranging from 52 to 70.9 from texts, tables, and figures of each included study, including: years. Nineteen studies (20, 21, 26–34, 36–43) included only first author, publication year, country, year of sample collection, men with penile SCC, and one study (35) included various age at diagnosis (mean, median, range), follow-up time, type of histologies of penile cancer, with the proportion of SCC being tissue, histology of cancer, tumor stage, tumor grade, lymph node 86%. The majority of studies (n ¼ 15; refs. 26–32, 35–39, 41–43) status, treatment modalities, HPV testing method, p16 testing included men with penile cancer with histologic grade 1–3 and technique, definition of p16 positivity (overexpression), number five studies (20, 21, 33, 34, 40) included penile cancers of grade 1 of evaluators of p16 staining, sample size, number of HPV- to 4. The majority of studies (n ¼ 12; refs. 20, 21, 29, 30, 32, 33, 35, positive and -negative penile cancers, number of p16-positive 38–42) included penile cancer stage I–IV. Three studies (20, 38, (overexpression) and p16-negative penile cancers, and survival 39) also comprised noninvasive tumor stages (Tis or Ta), which in end points. Different survival outcomes were examined, includ- total accounted for 36 of the 230 penile cancer cases included in ing: OS, disease-specific survival (DSS), and DFS. Studies report- these studies.
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