Transmission of gonorrhea from the oral cavity to the rectal tract: A systematic review

Abstract

Background

The antimicrobial resistance of Neisseria gonorrhoeae and the high prevalence of asymptomatic extragenital infections are a worldwide concern. This research investigated whether gonorrhea can be transmitted from the oral cavity to the anorectal tract among men who have sex with men.

Purpose

The aim of this research is to find plausible relationships regarding the probability of gonococcal transmission from the oral cavity to the anorectal tract among MSM.

Research Design

A research question was defined using the P.I.C.O. strategy (population, intervention or exposure, comparison and outcome), where the target population is MSM, the intervention is exposure to contaminated oral cavity/saliva, the control is the absence of exposure, and the outcome is the acquisition of GC. The eligibility criteria included observational studies involving men who have sex with men, regardless of sexual orientation, aged 16 or older, screened for oropharyngeal and rectal gonorrhea, and examining the role of oral fluids in transmission. Studies involving partners previously diagnosed with urogenital gonorrhea or reporting consistent condom use during receptive penoanal sex were excluded to avoid urethral-to-anorectal transmission bias.

Study Sample

The databases employed were PubMed, Scopus, Web of Science, EBSCO, SciELO, and the Virtual Health Library (VHL). A total of 383 studies were identified, however, only 6 were included.

Data Collection and/or Analysis

According to the Newcastle-Ottawa Scale (NOS), two studies were “very good,” two “good,” and two “satisfactory”. Most studies described a complete methodology according to Strengthening the Reporting of Observational studies in Epidemiology (STROBE).

Results

Differences in diagnostic methods, methodologies, and variables limited the findings. While the results do not confirm transmission from the oral cavity to the anorectal tract, they suggest its possibility. Further research is needed to better understand this transmission route.

Conclusions

Transmissibility of gonorrhea from oropharyngeal via to the anorectal tract cannot be totally establish. However, evidence suggested the existence of this gonorrhea transmission. The fact that men with rectal gonorrhea continue to appear, even in contexts of condom use or the absence of receptive penoanal sex, brings the importance of cases monitoring and the establishment of preventive strategies.

Keywords

Mouth rectum gonorrhoea sexually transmitted diseases sexual and gender minorities

Introduction

Gonorrhea (GC) is a sexually transmitted infection (STI) of worldwide concern, commonly reported and affecting individuals of all sexes.¹ The prevalence of gonorrhea is disproportionate among men who have sex with men (MSM).^2,3 In fact, oropharyngeal (OPG), anorectal (ARG) and urogenital gonorrhea (UGG) among MSM was reported to be 8.5%, 15.0% and 6.81% respectively.^4,5 Young individuals aged 24 years or younger and those with multiple casual sexual partners are most affected in this population.^2,6–8

Gonococcal transmission occurs through direct inoculation of infected secretions during sexual intercourse between three anatomical sites in individuals with penises: the urethra, oropharynx, and rectum.¹ Extragenital infections of GC are generally asymptomatic and potential transmitters^9,10 with high viable gonococcal loads^11–14 with the duration of untreated infections until spontaneous elimination being approximately four to 12 months.^15,16 Urethral infection, in turn, is generally symptomatic, with an incubation period of two to 8 days.^1,17–19

Among authors and international clinical protocols, there are various considerations regarding the modes of transmission (e.g., urethra - anus, anus - oropharynx, oropharynx - oropharynx). Current public health strategies in countries such as Brazil and the United States are based on the traditional paradigm that the urethra performs a central role in the transmission of gonorrhea, primarily through sexual practices.^20–22 Australia follows a different approach, proposing that the high prevalence of this infection is explained by the oropharynx as the primary source of transmission, that is, through saliva in situations such as French kissing and sexual practices (oral, orogenital, use of saliva as a lubricant, etc.).²³

The oropharynx may perform a crucial role in understanding the transmission of gonorrhea among MSM and its multiple antimicrobial resistances.²³ Most of these infections are asymptomatic, drug action at this site is less effective, and there is genetic material exchange of Neisseria gonorrhoeae (NG) with various commensal species of the same genus, including antibiotic resistance genes.²⁴ Genomic analyses have demonstrated that resistant strains are transmitted between sexual partners.²⁵ Discoveries indicate that NG can be cultured from rectal swabs, oropharyngeal swabs, and expectorated saliva in a significant proportion of patients positive for the infection at these sites, and that there is a substantial bacterial DNA load in these samples.^11,12,26 However, it is uncertain to what extent kissing and saliva contribute to the transmission of gonorrhea.^18,27

Little is known and discussed regarding the contributions of sexual practices involving the oral cavity and saliva in the transmission of NG,^13,28 which leads to the belief that they are safe and would not pose health risks,²⁸ except in the condition of visible and obvious lesions.²⁹ The effectiveness of interventions against transmission at each specific site is highly uncertain given the possibility of additional transmission routes.³⁰ This understanding is crucial for predicting the effectiveness of interventions.^12,30 Given the discovery of a considerable load of gonococci in saliva,^12,13 it is presumed that any sexual activities involving it, which are frequent among MSM,^28,29,31 may carry the infection. The aim of this research is to find plausible relationships regarding the probability of gonococcal transmission from the oral cavity to the anorectal tract among MSM.

Methodology

The present study constitutes a systematic review. A research question was defined using the P.I.C.O. strategy (population, intervention or exposure, comparison and outcome), where the target population is MSM, the intervention is exposure to contaminated oral cavity/saliva, the control is the absence of exposure, and the outcome is the acquisition of GC. The research question defined was: “Among men who have sex with men, can gonorrhea be transmitted from the oral cavity to the anorectal tract?”

The databases employed were PubMed, Scopus, Web of Science, EBSCO, SciELO, and the Virtual Health Library (VHL). Initially, a search pattern was established using Mesh terms, synonyms, and terms commonly used by authors, linked with Boolean connectors: (“neisseria gonorrhoeae” OR gonorrhoea OR gonococcal) AND (transmission OR sexual OR risk) AND (pharyngeal OR oropharyngeal OR pharynx OR oropharynx OR mouth OR saliva OR throat OR rimming OR anilingus OR “receptive anal practices”) AND (anal OR anorectal OR rectal OR anus) AND (“men who have sex with men” OR msm OR homosexual OR bisexual OR “gay men”). This pattern was employed and modified according to the specificities of each database, without limitations on date or language.

The search engines were organized according to a logical sequence: presenting results from studies on gonorrhea (1st group), its transmission or sexual risk factors associated with transmission (2nd group), infection in the oropharynx (3rd group), to the anorectal tract (4th group), among “men who have sex with men” (5th group). The expressions “rimming”, “anilingus”, and “receptive anal practices” were included to encompass studies relating these sexual risk practices to transmission. The term “men who have sex with men” (MSM) in the fifth group is the most recent, utilized, and appropriate for defining the sexual interest group of the research, given that sexual orientation (homosexual, bisexual, etc.) is subjective, although used in search engines as it was more commonly employed in the 20th century.

The eligibility criteria encompassed observational studies whose target population consisted of men from the group “men who have sex with men,” regardless of sexual orientation, aged 16 years or older, screened for oropharyngeal and rectal gonorrhea, and which investigated the involvement of oral cavity fluids in the transmission process. To exclude the possibility of infection from the urethra to the anorectal tract, studies that included groups of partners previously diagnosed with urogenital gonorrhea or with reports of consistent condom use for receptive penoanal sex were excluded.

Two reviewers conducted independent searches in the databases and determined the final sample based on an analysis of titles, abstracts, and full texts that met the eligibility criteria.

The quality of the studies included in the final sample was assessed using the Strengthening the Reporting of Observational studies in Epidemiology (STROBE) instrument and the Newcastle-Ottawa Scale (NOS). For data analysis, prevalence and incidence ratios of anorectal gonorrhea, oropharyngeal gonorrhea, and urogenital gonorrhea reported in the studies and the risk factors for the acquisition of GC were collected: partners diagnosed with oropharyngeal gonorrhea and practices including receptive anal sex, digital-anal or fisting, and oroanal activities, as well as the use of saliva as a lubricant. Additionally, confounding factors such as the number of sexual partners, HIV status, and condom use were collected. The data were organized, categorized, and analyzed using Excel spreadsheets and presented in tables and figures.

Results

The search results are detailed in Figure 1. A total of 1011 articles were found in the databases: Web of Science (174), Scopus (252), PubMed (269), EBSCO (95), and VHL (221). No results were obtained from searches in the SciELO database. After the removal of 628 duplicate studies, 383 remained. These were analyzed according to the eligibility criteria, resulting in a final analytic sample composed of six studies^18,32–36 with data reported in English language.

Figure 1.

Detailed search result.

Table 1 presents the results of the quality analysis using the STROBE and NOS instruments, which are specific to observational cohort and cross-sectional studies. According to the scale NOS, two studies^18,36 were rated as “very good” quality (nine stars), two^32,34 as “good” (seven stars), and two^33,35 as “satisfactory” (six stars). The results from STROBE indicate that five studies^{18,32,33,35,36} describe their methodology completely, while only one study³⁴ provided a partial description. Four studies^18,32,34,36 met the majority of the criteria for the analysis of results and discussion.

Table 1.

Quality analysis of studies according to STROBE and NOS criteria (score) for observational studies.

Strobe		Nos -Cohort/Cross-Sectional^a	Cornelisse, 2019^a,18	Cornelisse, 2018^a,35	Allan-Blitz, 2017³⁴	Chow, 2016^a,32	Jin, 2007³²	McMillan, 2000^a,34
1)Title	Study design		Yes	No	No	Yes	Yes	No
2)Abstract	Efficient summary of what was done and found		Yes	Yes	Yes	Yes	Yes	Yes
Introduction
3)Context/rationale	Explains scientific context and clear rationale		Yes	Yes	Yes	Yes	Yes	Yes
4)Objective	Pre-established hypotheses		Yes	Yes	Incomplete	Yes	Yes	Yes
Methods		Selection/Comparability/Outcome (☆)
5)Study design	Presents main elements	1) Cohort representativeness/sample^a	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)
6)Setting	Describes location, date, exposure, follow-up, and collection	2) Selection of non-exposed cohort/Sample size^a	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)
7)Participants	Eligibility criteria, sources, and selection methods	3) Determination of exposure/Non-respondents^a	Yes(☆)	Yes(−)	Yes(☆)	Yes(−)	Yes(☆)	Incomplete(−)
8)Variables	Clearly defines all outcomes, exposures, confounding factors, and effect modifiers. Provides diagnostic criteria, if applicable	4) The outcome of interest was not present at the beginning of the study/Validation of exposure (risk factors)^a	(☆)	(☆)	(−)	(☆)	(−)	(☆)
8)Data sources / Measurement	Clear definition of outcomes, exposure, predictors, potential confounders, effect modifiers, and diagnostic criteria	5) Control for major and additional confounding factors	Yes(☆☆)	Yes(☆☆)	Yes(☆☆)	Yes(☆☆)	Yes(☆☆)	No(☆)
9)Bias	Attempt to reduce bias	6) Outcome assessment	Yes(☆☆☆)	Yes(☆☆☆)	Yes(−)	Yes(☆)	Yes(−)	Yes(☆☆☆)
10)Study size	Explanation of the definition	7) The follow-up was sufficient for the occurrence of outcomes	Yes(−)	Yes(☆)	Yes(☆)	Yes(☆)	Yes(☆)	No(−)
11)Quantitative variables	Explains the analysis of quantitative variables and describes groupings	8)Adequacy of cohort follow-up/NA^a	Yes(NA)	Yes(NA)	Yes(−)	Yes(NA)	Yes(−)	No(NA)
12)Statistical methods	Describes statistical methods, confounding control, subgroup and interaction assessments, and sampling analyses		Yes	Yes	Yes	Yes	Yes	Descriptive
Results
13)Participants	Reports the number of individuals at each stage, justifies non-participants, and uses diagrams		Yes	Only does not use diagrams	Yes	Yes	Only does not use diagrams	No
14)Descriptive data	Demographic, clinical, and social data, exposure, and potential confounders		Yes	Yes	Yes	Yes	Yes	Yes
15)Outcome data	Reports number of events and summarized assessments		Yes	Yes	Yes	Yes	Yes	Yes
16)Main results	Unadjusted and adjusted estimates with precision (95% CI) and confounders		Unadjusted	Adjusted	Adjusted	Adjusted	Yes	No
17)Others analyses	Reports other analyses - subgroups, interactions, and sensitivity analysis		Genomic analysis	No	Risk factors	No	No	Genomic analysis
Discussion
18)Main results	Summarize key results relevant to the objectives		Yes	Yes	Yes	Yes	Yes	Yes
19)Limitations	Discusses limitations, direction, and magnitude of potential biases		Yes	Yes	Yes	Yes	No	Yes
20)Interpretation	Cautious interpretation, objective data, limitations, multiplicity of analyses, results from similar studies, and other relevant evidence		Yes	Yes	Yes	Yes	Yes	Yes
21)Generalization	Discusses the generalization of the results		Yes	Yes	Yes	Yes	No	Yes
Other information
22) Funding	Presents funding source or funders involved in the project		Yes	Yes	Yes	Yes	Yes	No
NOS TOTAL SCORE +			9	9	6	7	6	7

STROBE = Strengthening the Reporting of Observational Studies in Epidemiology. NOS = Newcastle-Ottawa Scale (NOS) for assessing the quality of observational studies.

^a = Cross-sectional studies.

+ = NOS Scores: 9–10 (Very good);7–8 (good); 5–6 (Satisfactory); 0–4 (Unsatisfactory).

NA = Not applicable.

Table 2 provides a qualitative description of the main methodological characteristics and outcomes of the studies that comprise the final sample. Most of the studies are cross-sectional,^18,32,34,36 while two are cohort studies.^33,35 Four of the studies were conducted in Australia^18,32,33,36 one in Peru³⁵ and one in Edinburgh.³⁴ Four studies^32,33,35,36 had a sample size greater than 150 participants.

Table 2.

Description of methodological characteristics and results of the final sample.

Authors and year	Study design	Country and Population	n	Age range (years)	Prevalence* /Incidence+ (%)	Sampling technique	Studied variables	Results
Cornelisse, 2019¹⁸ ☆☆☆☆☆☆☆☆☆	Cross-sectional	Australia	120 (60 couples)	Average = 30 (IQR 25–36)	OPG* = 6,2	Swabs from the oropharynx, anus, and urethra were collected for NAAT testing, with positive samples further tested using culture	Age, HIV status, number of casual sexual partners, gonorrhea positivity, sexual practice (passive/active) with/without condom use (last 3 months)	Among the couples, at least one had gonorrhea, and isolates in culture showed high phylogenetic relatedness between partners. After excluding men with UGG, among 32 men with ARG, 34% of them had partners with OPG among the 48 couples with partners without UGG, 23% of them both had OPG. There was no urethral infection in partners of men with OPG and ARG
Cornelisse, 2019¹⁸ ☆☆☆☆☆☆☆☆☆	Cross-sectional	Adult men	120 (60 couples)	Average = 30 (IQR 25–36)	ARG* = 2,9
Cornelisse, 2018³⁶ ☆☆☆☆☆☆☆☆☆	Cross-sectional	Australia	990 (495 couples)	Average = 18 (IQR 24–34)	PHG* = 2,6	Swab in oropharynx, anus, and urethra for culture testing	Age, HIV status, symptoms, sexual position, number of sexual partners, and sexual activity with/without condom use (last 3 months)	Of the 33 men with UGG, 33% had partners with OPG and 67% had partners with ARG. The probability of acquiring UGG was 4.6 (95% CI 1.2–17.1) for partners with OPG and 48.1 (95% CI 18.3–126.7) for partners with ARG. Of the 26 men with OPG, 42% had partners with ARG and 23% had a partner with OPG. The probability of acquiring OPG was 18.3 (95% CI 6.9–48.8) for partners with UGG and 8.9 (95% CI 3.2–24.6) for partners with ARG. Of the 48 men with ARG, 46% had partners with UGG and 23% had partners with OPG. The probability of having ARG was 63.9 (95% CI 24.7–165.6) for partners with UGG; 3.4 (95% CI 1.0–12.2) for partners with OPG, and 6.9 (95% CI 2.4–20.3) for partners with ARG.
		Australia			ARG* = 4,8
		Adult men			UGG* = 3,3
Allan-Blitz, 2017³⁵ ☆☆☆☆☆☆	Cohort	Peru	404	Average = 29,6	ARG+ = 28,1	Swab in pharynx, urethra, and anus for NAAT testing	Age; income, HIV; treatment center, number of partners; alcohol/drug use before sex; antibiotics; transgender identity; sexual position; sexual practice – penoanal, oropenian oroanal – active/passive with/without condom (last 6 months)	The incidence of ARG was associated with HIV (aIRR 2.43; 95%CI 1.66–3.55), being versatile (aIRR 5.23; 95%CI 1.89–14.44), being passive (aIRR 4.51; 95%CI 1.60–12.75), and identifying as transgender women (aIRR 2.43; 95% CI 1.66–3.55), which was also associated with CO (aIRR 2.66; 95%CI 1.45–4.88). RC was associated with being passive (1.93; 95%CI 1.07–3.49), being versatile (aIRR 1.62; 95%CI 0.91–2.89), and the number of sexual partners (>4–9) (aIRR 1.80; 95%CI 1.19–2.73)
		Adult men			CO+ = 7,3
					OPG+ = 21,3
					CO+ = 9,6
Chow, 2016³² ☆☆☆☆☆☆☆	Cross-sectional	Australia	1312	17–78 (Median 29; IQR 25–37)	ARG* = 4,3	Pharynx and anal swabs were taken from all participants, and urethral swabs were taken from symptomatic cases. Culture test was performed	Age, HIV status, number of partners, oropharyngeal gonorrhea, partner’s saliva use in sexual practices (anal, passive oroanal, digital-anal, and active/passive penis dipping, with/without condom use	Gonorrhea (GR) was associated with saliva use as lubricant (aOR 2.17; 95% CI 1.00–4.71), inconsistent condom use (aOR 2.66; 95% CI 1.42–4.97), receptive oral-anal sex (aOR 17.31; 95% CI 6.29–47.63), HIV positivity (aOR 6.23; 95% CI 2.27–17.10), age group ≤24 years (aOR 4.93; 95% CI 1.83–13.27; p < .002), and age Group 25–34 years (aOR 3.63; 95% CI 1.43–9.24). Excluding urethral involvement, OPG was associated with ARG, through saliva use as lubricant
Chow, 2016³² ☆☆☆☆☆☆☆	Cross-sectional	Adult men	1312	17–78 (Median 29; IQR 25–37)	OPG* = 1,7
Jin, 2006³³ ☆☆☆☆☆☆	Cohort	Australia	1427	18–75 (Median 35)	UGG+ = 3,49	Swab in anus and urine samples in NAAT	Age, number of casual partners, sex with a man positive for PHG, contact’s HIV history, sexual practices (oropenile, digital-anal, oroanal, fisting, and dildo use; active/passive) with/without condom), sexual position (last 6 months)	The incidence of ARG was associated with a sexual partner with gonorrhea (aHR 5.59, 95%CI 3.24–9.64); passive penoanal sex without a condom and without ejaculation (aHR 2.15; 95%CI 1.21–3.79) or with ejaculation (aHR 3.48, 95%CI 1.91–6.37), and digital-anal sex (aHR 4.58, 95%CI 2.26–9.28). ARG in the group that reported not having engaged in passive penoanal sex without a condom was associated with digital-anal (p_trend = 0.002), fisting (p_trend = 0.001), and oroanal (p_trend = 0.001) sexual practices. The incidence of GU was associated with a sexual partner with gonorrhea (aHR 4.14, 95%CI 2.44–7.04); number of sexual partners (aHR 2.39, 95%CI 1.35–4.21), and having a partner with HIV (aHR 2.58, 95%CI 1.10–6.05). The incidence of RC was associated with a sexual partner with chlamydia (aHR 2.10; 95%CI 1.48–4.94); number of sexual partners >50 (aHR 2.12, 95%CI 1.16–3.90), passive penoanal sex without a condom and without ejaculation (aHR 2.62, 95%CI 1.69–4.06), with ejaculation (aHR 2.98, 95%CI 1.76–5.02); and passive oroanal sex occasionally (aHR 2.07, 95%CI 1.19–3.61) and always (aHR 2.53, 95%CI 1.35–4.76). The incidence of UC was associated with contact with chlamydia (aHR 4.61, 95%CI 3.07–6.92), more than 11 sexual partners (aHR 1.49, 95%CI 1.01–2.19); penoanal sex without a condom in the versatile position (aHR 1.61, 95%CI 1.10–2.35), and oropenile sex with ejaculation (aHR 1.54, 95%CI 1.13–2.11). HIV was associated with UGG.
		Adult men			ARG+ = 2,96
					UC+ = 7,43
					RC+ = 4,98
McMillan, 2000³⁴ ☆☆☆☆☆☆☆	Cross-sectional	Edinburgh	141	14–56 (median 26)	-	Swab in anus, urethra, and oropharynx (tonsils) for culture testing	Age; number of sexual partners; condom use for passive penoanal intercourse; symptoms in the anus or urethra; contact with a partner diagnosed with gonorrhea of the throat; health exams; auxotype/serotype comparison with contacts (last 3 months)	There were 155 episodes of infection: 141 had one episode, 12 had two episodes, and 1 had three episodes. Among the likely sources of infection in 46 index cases with ARG, the urethra was the most commonly infected site (72%), either individually or simultaneously with infection at another site. The presence of only oropharyngeal infection was detected in 20% of the 46 cases, of which 3 reported a history of condom use. 11 out of 12 NG isolates from the patients’ oropharynx matched the same auxotype/serotype as the index cases of ARG.
McMillan, 2000³⁴ ☆☆☆☆☆☆☆	Cross-sectional	Adult men and adolescents with ARG	141	14–56 (median 26)	-	Gram stain analysis on urethral discharge smear, serotype, and auxotype

OPG = Oropharyngeal gonorrhea, ARG = Anorectal gonorrhea, UGG = Urogenital gonorrhea, UC = Urethral chlamydia, RC = Rectal Chlamydia, NAAT = Nucleic acid amplification test, CI = Confidence interval, OR = Odds Ratio, aOR = Adjusted Odds ratio, aIRR = Adjusted incidence rate, aHR = Adjusted risk ratio.

In this sample, the prevalences found for anorectal gonorrhea ranged from 2.9% to 4.8%, for oropharyngeal gonorrhea from 1.7% to 6.2%, and for urogenital gonorrhea was 3.3%. Meanwhile, the incidences for anorectal gonorrhea ranged from 3.0 to 28.1 cases per 100 person-years, for oropharyngeal gonorrhea was 21.3 cases per 100 person-years, and for urogenital gonorrhea was 3.5 cases per 100 person-years. In two studies,^32,35 the presence of anorectal gonorrhea was associated with HIV in the same individual.

Four studies^18,32,34,36 analyzed sexual risk practices for gonorrhea. One study³² found an association with the use of saliva during penoanal sexual practice conducted in the 3 months prior to testing, and another³³ with digital-anal, fisting, and oroanal practices in the 6 months prior. In two articles,^32,33 gonorrhea was significantly associated with unprotected penoanal sexual practice.

Three studies^32,33,35 sought evidence regarding the transmission of gonorrhea from the oral cavity to the anus (oropharyngeal gonorrhea to anorectal gonorrhea). In these studies, three sites (anorectal tract, oropharynx, and urethra) were screened in couples to detect extragenital infections that could not have been caused by urethral infection, and to determine if among these partners there would be the presence of anorectal gonorrhea and oropharyngeal gonorrhea, but without urogenital gonorrhea. It was demonstrated in all three studies that in the absence of urethral infection, men with anorectal gonorrhea commonly had partners with oropharyngeal gonorrhea; however, the studies did not indicate the direction of transmission. Two studies^32,35 conducted phylogenetic analyses of strains isolated from sexual partners positive for oropharyngeal gonorrhea and anorectal gonorrhea and found a high concordance between the pairs.

Discussion

In the current study, half of the investigations demonstrate that men with anorectal gonorrhea had steady partners with oropharyngeal gonorrhea, excluding the involvement of urogenital gonorrhea.^18,34,36 These studies did not seek to identify the origin of the infection; however, it was assumed that the direction of transmission is from mouth to anorectal tract. This hypothesis is supported by a previous study by Cornelisse et al.,,²⁷ in which no association was found between active oroanal sex as a risk factor for oropharyngeal gonorrhea, and other evidence of detection and cultivation of NG in saliva samples,^12,13 a frequent element in practices among MSM.^{28,29,31,37,38}

In our sample, two studies identified an association between anorectal gonorrhea and the use of saliva³² or the oral cavity during sexual practices.³³ Jin et al.,³³ did not include saliva in their analysis, whereas Chow et al.,³² when including saliva, did not detect a significant association value for oroanal sex. Studies discussed that the volume of infected saliva introduced into the anorectal tract by the tongue during oroanal sexual practice or by penile or digital penetration with saliva lubrication could be responsible for this transmission.^28,32,37,38

The involvement of saliva in sexual practices is an important factor for discussions on sexual health, as it contains various microorganisms, including NG, and its presence is particularly notable in relationships among men, whether due to kissing, the use of saliva as an anal lubricant, oroanal sex, or other sexual fetishes such as spitting during the sexual act (knowing as “sialophilia”). Studies have discussed the role of saliva in the rectal transmission of the disease, commonly active in sex among MSM, which can come into direct contact with the anus in large quantities.^28,37,38 Fairley et al.,²³ proposed that the incidence of anorectal gonorrhea among MSM could occur due to the involvement of saliva in ororectal sex or as a lubricant, practices common among MSM.^28,29,31,37

In our study, prevalences reported for anorectal gonorrhea, oropharyngeal gonorrhea and urogenital gonorrhea were low. Studies that focus in oral transmission of gonorrhea reported similar results. For instance, pharyngeal, urethral, and anal gonorrhea was reported to be 1.7%, 2.3%, and 2.9%, respectively³⁹ and 3.8%, 2.3% and 0% at oropharynx , anorectum and urethra.⁴⁰ These results could be related to the relatively short lived of the bacteria in oropharyngeal sites reported to be clear in approximately 6 weeks to 12 weeks. Thus, lower prevalences by oral transmission, for example by kissing, were expected.⁴⁰

On the other hand, studies have identified higher prevalences of asymptomatic gonorrhea at extragenital sites^3,9,41,42 compared to urogenital gonorrhea. Furthermore, the acquisition of anorectal gonorrhea still occurs in a scenario of frequent condom use for anal sex,⁴³ and studies have reported these findings. According to the authors, the increase in disease cases cannot be explained solely by urethral transmission, and most infections would not be identified if screening were conducted only for urogenital gonorrhea or based on symptoms or sexual history.^41,44–46 Ong et al.,¹⁷ found in their research that 11% of urethral infections would be missed if only symptomatic cases were diagnosed. Marcus et al.,⁴⁶ reported that with exclusive urethral screening, the loss of gonorrhea cases was high (95.2%). All this reinforces the paradigm proposed by Fairley et al.,,²³ in which oropharyngeal gonorrhea would be the main culprit for the transmission of GC at the three sites, including the oropharynx.

Biopsychosocial factors, such as the culture in each country or region, can influence outcomes. For instance, in the metropolitan region of Australia³² and in San Francisco, United States,²⁸ studies indicate that oroanal sex and the use of saliva as a lubricant are common practices among MSM. Additionally, a younger age, below 35 years, can also be a risk factor associated with GC.^47,48

There remains a limited number of studies with research samples that constitute a small analysis pool. The discussion regarding the origin of anorectal gonorrhea began in 1991 with Tomlinson et al.,,⁴⁹ but it was not until 2000³⁴ that the first article based on this inquiry was published. The second study was released in 2007,³³ but it took another 9 years for a new investigation to emerge. From 2016 to 2019, a study was published each year^18,32,35,36; however, no further studies have been conducted since then.

Studies found that having more than one partner in the last 3 months and among seropositive HIV patients increased the risk of gonorrhea.⁵⁰ On the other hand, studies^50,51 showed that the use of condom during intercourse reduced the risk of having gonorrhea by almost 61%.⁵⁰ In our study, these confounding factors were collected to reduce bias. However, considering the nature of such information, there exists the possibility of inaccurate responses.

Several limitations can be noted. There is a need for standardization in diagnostic methods and methodologies used across studies. Some used culture methods, while others utilized NAAT techniques. Compared to culture, NAAT techniques have higher sensitivity in detection, which could lead to differences in the value of the associations found.^52–54 Most studies include various variables, with no reports of standardized instruments being used. Another limitation is the exposure time employed in the sexual history of participants. Anorectal gonococcal infections are commonly asymptomatic, lasting approximately 12 months until complete resolution by the immune system,¹⁶ thus making it impossible to estimate the duration of the infection until diagnosis. Therefore, data collection in cross-sectional studies over a shorter interval could be subject to variations.

Given the higher prevalence of extragenital gonorrhea among MSM,^3,9,41,42 there is a public health concern, particularly in countries where these cases are not routinely identified or where detection relies solely on self-reported sexual behaviors. To confirm oral-to-anal transmission, future research should prioritize well-designed longitudinal studies that incorporate microbiological typing methods, such as whole-genome sequencing, to establish transmission pathways. Additionally, studies should systematically collect behavioral data, including detailed sexual practices, partner networks, and frequency of exposures, alongside biological sampling from multiple anatomical sites over time. Standard methods that include more specific and validated tools, to collect data such as risk variables, are recommended to achieve more precise results and a better comprehension of disease in that risk population.

Conclusion

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Yuri Garcia Dutra Souza

Yan Rocha Neves

Valéria de Oliveira

Luiz Eduardo de Almeida

Mabel Miluska Suca Salas

References

Bignell

Unemo

European STI Guidelines Editorial Board

2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS 2013; 24(2): 85–92.

Templeton

Jin

McNally

, et al. Prevalence, incidence and risk factors for pharyngeal gonorrhoea in a community-based HIV-negative cohort of homosexual men in Sydney, Australia. Sex Transm Infect 2010; 86(2): 90–96.

Comninos

Garton

Guy

, et al. Increases in pharyngeal Neisseria gonorrhoeae positivity in men who have sex with men, 2011-2015: observational study. Sex Transm Infect 2020; 96(6): 432–435.

Calas

Zemali

Camuset

, et al. Prevalence of urogenital, anal, and pharyngeal infections with Chlamydia trachomatis, Neisseria gonorrhoeae, and Mycoplasma genitalium: a cross-sectional study in Reunion island. BMC Infect Dis 2021; 21(1): 95.

Bamberger Dm Fau - Graham

Graham

Fau - Dennis

, et al. Extragenital gonorrhea and Chlamydia among men and women according to type of sexual exposure, Sex Transm Dis 2019; 46(5): 329–334.

Barbosa

Moherdaui

Pinto

, et al. Prevalence of Neisseria gonorrhoeae and Chlamydia trachomatis infection in men attending STD clinics in Brazil. Rev Soc Bras Med Trop 2010; 43(5): 500–503.

Pattanasin

Dunne

Wasinrapee

, et al. Screening for Chlamydia trachomatis and Neisseria gonorrhoeae infection among asymptomatic men who have sex with men in Bangkok, Thailand. Int J STD AIDS 2018; 29(6): 577–587.

Tao

Hoover

Nye

, et al. Rectal infection with Neisseria gonorrhoeae and Chlamydia trachomatis in men in the United States. Clin Infect Dis 2016; 63(10): 1325–1331.

Passaro

Segura

Perez-Brumer

, et al. Body parts matter: social, behavioral, and biological considerations for urethral, pharyngeal, and rectal gonorrhea and Chlamydia screening among MSM in Lima, Peru. Sex Transm Dis 2018; 45(9): 607–614.

10.

Jiddou

Alcaide

Rosa-Cunha

, et al. Pharyngeal gonorrhea and chlamydial infections in men who have sex with men, a hidden threat to the HIV epidemic. Journal of Therapy and Management in HIV Infection 2013; 1(1): 19–23.

11.

Bissessor

Whiley

Lee

, et al. Detection of Neisseria gonorrhoeae isolates from tonsils and posterior oropharynx. J Clin Microbiol 2015; 53(11): 3624–3626.

12.

Chow

Lee

Tabrizi

, et al. Detection of Neisseria gonorrhoeae in the pharynx and saliva: implications for gonorrhoea transmission. Sex Transm Infect 2016; 92(5): 347–349.

13.

Chow

Tabrizi

Phillips

, et al. Neisseria gonorrhoeae bacterial DNA load in the pharynges and saliva of men who have sex with men. J Clin Microbiol 2016; 54(10): 2485–2490.

14.

Ratnappuli

Bissessor

Arumugam

, et al. Culture obtained from urethral swab of asymptomatic men who screen positive for Neisseria gonorrhoeae by urine nucleic acid amplification testing. Sex Transm Infect 2022; 98(2): 139–141.

15.

Barbee

Soge

Khosropour

, et al. The duration of pharyngeal gonorrhea: a natural history study. Clin Infect Dis 2021; 73(4): 575–582.

16.

Chow

Camilleri

Ward

, et al. Duration of gonorrhoea and chlamydia infection at the pharynx and rectum among men who have sex with men: a systematic review. Sex Health 2016; 13(3): 199–204.

17.

Ong

Fethers

Howden

, et al. Asymptomatic and symptomatic urethral gonorrhoea in men who have sex with men attending a sexual health service. Clin Microbiol Infect 2017; 23(8): 555–559.

18.

Cornelisse

Williamson

Zhang

, et al. Evidence for a new paradigm of gonorrhoea transmission: cross-sectional analysis of Neisseria gonorrhoeae infections by anatomical site in both partners in 60 male couples. Sex Transm Infect 2019; 95(6): 437–442.

19.

Ryder

Lockart

Bourne

. Is screening asymptomatic men who have sex with men for urethral gonorrhoea worthwhile? Sex Health 2010; 7(1): 90–91.

20.

Bachmann

Chan

Johnston

, et al. Sexually transmitted infections treatment guidelines. Geneva: World Health Organization, 2021, pp. 1545–8601.

21.

Fairley

Hocking

Zhang

, et al. Frequent transmission of gonorrhea in men who have sex with men. Emerg Infect Dis 2017; 23(1): 102–104.

22.

Lannoy

Silva

RJC

Nahn Júnior

, et al. Protocolo Brasileiro para Infecções Sexualmente Transmissíveis 2020: infecções que causam corrimento uretral. Epidemiol Serv Saúde 2021; 30(spe1): 2021.

23.

Fairley

Hocking

Zhang

, et al. Frequent transmission of gonorrhea in men who have sex with men. Emerg Infect Dis 2017; 23(1): 102–114.

24.

Kenyon

Osbak

. Certain attributes of the sexual ecosystem of high-risk MSM have resulted in an altered microbiome with an enhanced propensity to generate and transmit antibiotic resistance. Med Hypotheses 2014; 83(2): 196–202.

25.

Kwong

Chow

EPF

Stevens

, et al. Whole-genome sequencing reveals transmission of gonococcal antibiotic resistance among men who have sex with men: an observational study. Sex Transm Infect 2018; 94(2): 151–157.

26.

Hutt

Judson

. Epidemiology and treatment of oropharyngeal gonorrhea. Ann Intern Med 1986; 104(5): 655–658.

27.

Cornelisse

Walker

Phillips

, et al. Risk factors for oropharyngeal gonorrhoea in men who have sex with men: an age-matched case-control study. Sex Transm Infect 2018; 94(5): 359–364.

28.

Butler

Osmond

Jones

, et al. Use of saliva as a lubricant in anal sexual practices among homosexual men. J Acquir Immune Defic Syndr (1999) 2009; 50(2): 162–167.

29.

Nguyen

, et al. Prevalence and risk factors associated with HIV infection among men having sex with men in Ho Chi Minh City, Vietnam. AIDS Behav 2008; 12(3): 476–482.

30.

Spicknall

Mayer

Aral

, et al. Assessing uncertainty in an anatomical site-specific gonorrhea transmission model of men who have sex with men. Sex Transm Dis 2019; 46(5): 321–328.

31.

Richters

Zou

De Visser

, et al. Sexual health and behaviour of men in new south wales 2013-2014: school of public health and community medicine. Kensington: University of New South, 2015.

32.

Chow

EPF

Cornelisse

Read

TRH

, et al. Saliva use as a lubricant for anal sex is a risk factor for rectal gonorrhoea among men who have sex with men, a new public health message: a cross-sectional survey. Sex Transm Infect 2016; 92(7): 532–536.

33.

Jin

Prestage

Mao

, et al. Incidence and risk factors for urethral and anal gonorrhoea and chlamydia in a cohort of HIV-negative homosexual men: the Health in Men Study. Sex Transm Infect 2007; 83(2): 113–119.

34.

McMillan

Young

Moyes

. Rectal gonorrhoea in homosexual men: source of infection. Int J STD AIDS 2000; 11(5): 284–287.

35.

Allan-Blitz

Konda

Calvo

, et al. High incidence of extra-genital gonorrheal and chlamydial infections among high-risk men who have sex with men and transgender women in Peru. Int J STD AIDS 2018; 29(6): 568–576.

36.

Cornelisse

Zhang

Law

, et al. Concordance of gonorrhoea of the rectum, pharynx and urethra in same-sex male partnerships attending a sexual health service in Melbourne, Australia. BMC Infect Dis 2018; 18(1): 95.

37.

Chow

Cornelisse

Read

, et al. Saliva use in sex: associations with use of smartphone dating applications in men who have sex with men. Int J STD AIDS 2018; 29(4): 362–366.

38.

Lee

Gaither

Langston

, et al. Lubrication practices and receptive anal sex: implications for STI transmission and prevention. Sex Med 2021; 9(3): 100341.

39.

Chow

Tomnay

Fehler

, et al. Substantial increases in chlamydia and gonorrhea positivity unexplained by changes in individual-level sexual behaviors among men who have sex with men in an Australian sexual health service from 2007 to 2013. Sex Transm Dis 2015; 42(2): 81-87.

40.

Chow

EPF

Cornelisse

Williamson

, et al. Kissing may be an important and neglected risk factor for oropharyngeal gonorrhoea: a cross-sectional study in men who have sex with men. Sex Transm Infect 2019; 95(7): 516–521.

41.

Patton

Kidd

Llata

, et al. Extragenital gonorrhea and chlamydia testing and infection among men who have sex with men--STD Surveillance Network, United States, 2010-2012. Clin Infect Dis 2014; 58(11): 1564–1570.

42.

Gunn

O'Brien

Lee

, et al. Gonorrhea screening among men who have sex with men: value of multiple anatomic site testing, San Diego, California, 1997-2003. Sex Transm Dis 2008; 35(10): 845–848.

43.

Hui

Fairley

Chen

, et al. Oral and anal sex are key to sustaining gonorrhoea at endemic levels in MSM populations: a mathematical model. Sex Transm Infect 2015; 91(5): 365–369.

44.

Hiransuthikul

Sungsing

Jantarapakde

, et al. Correlations of chlamydia and gonorrhoea among pharyngeal, rectal and urethral sites among Thai men who have sex with men: multicentre community-led test and treat cohort in Thailand. BMJ Open 2019; 9(6): e028162.

45.

van Liere

Hoebe

Dukers-Muijrers

. Evaluation of the anatomical site distribution of chlamydia and gonorrhoea in men who have sex with men and in high-risk women by routine testing: cross-sectional study revealing missed opportunities for treatment strategies. Sex Transm Infect 2014; 90(1): 58–60.

46.

Marcus

Bernstein

Kohn

, et al. Infections missed by urethral-only screening for chlamydia or gonorrhea detection among men who have sex with men. Sex Transm Dis 2011; 38(10): 922–924.

47.

León

Konda

Klausner

, et al. Chlamydia trachomatis infection and associated risk factors in a low-income marginalized urban population in coastal Peru. Rev Panam Salud Publica 2009; 26(1): 39–45.

48.

Gálvez-Buccollini

DeLea

Herrera

, et al. Sexual behavior and drug consumption among young adults in a shantytown in Lima, Peru. BMC Public Health 2009; 9: 23.

49.

Tomlinson

French

Harris

, et al.

Does rectal gonorrhoea reflect unsafe sex?

Lancet (London, England) 1991; 337(8739): 501–502.

50.

Budkaew

Chumworathayi

Pientong

, et al. Prevalence and factors associated with gonorrhea infection with respect to anatomic distributions among men who have sex with men. PLoS One 2019; 14(4): e0211682.

51.

Warner

Newman

Austin

, et al. Condom effectiveness for reducing transmission of gonorrhea and chlamydia: the importance of assessing partner infection status. Am J Epidemiol 2004; 159(3): 242–251.

52.

Schachter

Moncada

Liska

, et al. Nucleic acid amplification tests in the diagnosis of chlamydial and gonococcal infections of the oropharynx and rectum in men who have sex with men. Sex Transm Dis 2008; 35(7): 637–642.

53.

Cornelisse

Chow

Huffam

, et al. Increased detection of pharyngeal and rectal gonorrhea in men who have sex with men after transition from culture to nucleic acid amplification testing. Sex Transm Dis 2017; 44(2): 114–117.

54.

Barbee

Dombrowski

Kerani

, et al. Effect of nucleic acid amplification testing on detection of extragenital gonorrhea and chlamydial infections in men who have sex with men sexually transmitted disease clinic patients. Sex Transm Dis 2014; 41(3): 168–172.