Increased likelihood of bacterial pathogens in the coronal sulcus and urethra of uncircumcised men in a diverse group of HIV infected and uninfected patients in India

Abstract

Background:The biological mechanism of circumcision as potentiating HIV prevention is poorly understood. Foreskin microbiota has been postulated as having a potential role; however, little is known about the relationship between bacterial pathogens and circumcision in adults.Materials and Methods:We sampled the coronal sulcus of a diverse group of circumcised and uncircumcised men (n=315) from a government chest hospital and fertility clinic in Hyderabad, Andhra Pradesh, India. Genital examination was conducted on three groups of men: Group 1 – HIV infected; Group 2 – TB infected; Group 3 – control. Aerobic and anaerobic specimens were cultured according to standard clinical protocols, and results were analyzed following multivariate logistic regression models.Results:Three hundred fifteen study participants – 47.6% of Group 1, 36.5% of Group 2, and 15.9% of Group 3 – were enrolled in the study and included in all analyses. Overall 37.1% of the participants were circumcised without variation across groups (P=0.29). Smegma was observed in 18.7% of the participants with no cases observed in Group 3 (P<0.001). Gram-negative pathogens were more prevalent among study participants in Group 1 (22.7%) and Group 2 (30.4%) as compared with those in Group 3 (6.0%) (P=0.003). In multivariate regression analysis, controlling for group, age, and presence of smegma, uncircumcised men were more likely to be colonized with gram positives [Adjusted Odds Ratio (AOR) 1.9; P<0.05)], gram negatives (AOR 2.4; P<0.05), or any pathogen (AOR 2.8; P<0.005).Conclusions:Uncircumcised men in this population in South India are more likely to harbor bacterial pathogens in the coronal sulcus than do their circumcised counterparts. Future studies should examine the relationship between foreskin microbiota and HIV transmission.

The penile microbiota of Black South African men: relationship with human papillomavirus and HIV infection

“…The distinct CSTs observed in the current study may relate to differences in penile moisture, sebum levels and oxygen availability. The penis provides several microenvironments that differ in levels of moisture, sebum and oxygen that may support distinct microbiota [5,12,14,26,27,36]. The coronal sulci and distal urethra, for example, were found in young adolescent men to harbor distinct bacterial communities [36].…”

“…Male circumcision has been found to alter the penile microbiome by significantly reducing bacterial diversity and load [12,13]. Pathogenic bacteria and dysbiosis in the penile microbiota, characterised by the presence of bacterial vaginosis (BV)-associated anaerobic bacteria such as Prevotella, have been identified as a key risk factor for HIV acquisition in uncircumcised men [5,14]. Several recent studies [15][16][17][18][19][20][21][22] have indicated that specific genital bacteria, which are more prevalent or abundant in uncircumcised men, could stimulate local immune responses that enhance epithelial inflammation and HIV target cell recruitment.…”

The Penile Microbiota in Uncircumcised and Circumcised Men: Relationships With HIV and Human Papillomavirus Infections and Cervicovaginal Microbiota

“…Lately, there has been considerable discussion regarding the genital microbiota of couples (41,70,71,106) and recognition that BV-associated bacteria may be sexually transmitted between partners (70)(71)(72)(106)(107)(108)(109). The penis of sexually-experienced and inexperienced men can be a reservoir of BV-associated bacteria (25,40,41,53,57,(70)(71)(72)(73) and other bacterial pathogens (3,4), which are often reduced by male circumcision (40,41,57). The penile bacteria may perhaps influence BV status in the female sexual partner (70,71).…”

“…Although it is well-documented that the human body is uniquely inhabited by site-specific microbiota (1,2), information on the penile (glans, coronal sulcus, foreskin, and shaft) microbiota remains remarkably deficient. Initial investigation of the penile bacteria relied on classical approaches such as culture (3,4). A caveat to the culture method is that about 99% of microorganisms discovered to date are yet to be cultured (5).…”

Microbiome in Human Immunodeficiency Virus Infection

“…Foreskin inflammation manifested by massive infiltrates of CD4 and CD8 T cells increases HIV infection 84 . Male circumcision significantly reduces the bacterial load, prevalence of some but not all anaerobic bacteria, and reduces microbiota diversity and composition 85, 86 . Studies have clearly shown that circumcision reduces the risk of HIV acquisition and bacterial and viral sexually transmitted infections (STIs) 87, 88 ; however, the underlying mechanism remains to be defined.…”