This systematic review aimed to explore any demographic, biological and behavioural characteristics of men who have sex with men (MSM) with diarrhoeagenic E.coli.
Design/Methods
We searched MEDLINE, EMBASE, and CINAHL for manuscripts published to March 2024. One author screened manuscript abstracts; two authors independently conducted a full text review. We only included primary data on gastrointestinal E.coli in MSM. Risk of bias was assessed independently by two authors using the Joanna Briggs Institute tools. This review was registered on PROSPERO(CRD42023455321).
Results
Eleven manuscripts (cross-sectional studies (n = 8), case-series (n = 1), case-control study (n = 1), longitudinal study (n = 1)) from Europe (n = 7) Australia (n = 2), USA (n = 2) including 983 MSM with gastrointestinal E.coli published between 2014–2023 were included in this review. Demographic factors (living with HIV, using HIV-PrEP, using dating apps and working as airline crew, group sex, non-regular (casual) sexual partners); behavioural factors (non-regular sexual partners, non-condom use, oro-anal sex, penile-anal sex, use of sex toys, insertive and receptive fisting, scat play); and infection factors (co-infection with Chlamydia trachomatis including LGV, Neisseria gonorrhoeae, Treponema pallidum, hepatitis C, other enteric pathogens [Shigella spp. Giardia duodenalis, Entamoeba histolytica, hepatitis A and intestinal spirochaetosis]) were observed in MSM with E. coli. Antimicrobial resistance (extended spectrum beta-lactamase and quinolone resistance) was described in MSM with E.coli.
Conclusion
We have highlighted demographic, behavioral and infection factors observed in MSM with E.coli suggesting sexual transmissibility. These data provide insight for future clinical guidelines, public health control strategies and research.
NewellDGLa RagioneRM. Enterohaemorrhagic and other Shiga toxin-producing Escherichia coli (STEC): where are we now regarding diagnostics and control strategies?Transbound Emerg Dis2018; 65 Suppl 1(Suppl 1): 49–71.
2.
JosephACointeAMariani KurkdjianP, et al.Shiga toxin-associated hemolytic uremic syndrome: a narrative review. Toxins2020; 12(2).
3.
JesserKJLevyK. Updates on defining and detecting diarrheagenic Escherichia coli pathotypes. Curr Opin Infect Dis2020; 33(5): 372–380.
4.
LanRAllesMCDonohoeK, et al.Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infect Immun2004; 72(9): 5080–5088.
5.
SoysalNMariani-KurkdjianPSmailY, et al.Enterohemorrhagic Escherichia coli Hybrid pathotype O80:H2 as a new therapeutic challenge. Emerg Infect Dis2016; 22(9): 1604–1612.
6.
RodwellEVSimpsonAChanYW, et al.The epidemiology of Shiga toxin-producing Escherichia coli O26:H11 (clonal complex 29) in England, 2014-2021. J Infect2023; 86(6): 552–562.
7.
Robins-BrowneRMHoltKEIngleDJ, et al.Are Escherichia coli pathotypes still relevant in the era of whole-genome sequencing?Front Cell Infect Microbiol2016; 6: 141.
8.
BakerKSDallmanTJFieldN, et al.Horizontal antimicrobial resistance transfer drives epidemics of multiple Shigella species. Nat Commun2018; 9(1): 1462.
9.
LozanoRNaghaviMForemanK, et al.Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet2012; 380(9859): 2095–2128.
HarroCChakrabortySFellerA, et al.Refinement of a human challenge model for evaluation of enterotoxigenic Escherichia coli vaccines. Clin Vaccine Immunol2011; 18(10): 1719–1727.
12.
DuPontHLLevineMMHornickRB, et al.Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis1989; 159(6): 1126–1128.
13.
AshidaAMatsumuraHSawaiT, et al.Clinical features in a series of 258 Japanese pediatric patients with thrombotic microangiopathy. Clin Exp Nephrol2018; 22(4): 924–930.
14.
KimmittPTHarwoodCRBarerMR. Toxin gene expression by shiga toxin-producing Escherichia coli: the role of antibiotics and the bacterial SOS response. Emerg Infect Dis2000; 6(5): 458–465.
15.
GreigDRDo NascimentoVOlonadeI, et al.Surveillance of antimicrobial resistant Shiga toxin-producing E. coli O157:H7 in England, 2016-2020. J Antimicrob Chemother2023; 78(9): 2263–2273.
16.
PoirelLMadecJYLupoA, et al.Antimicrobial resistance in Escherichia coli. Microbiol Spectr2018; 6(4).
17.
MitchellHHughesG. Recent epidemiology of sexually transmissible enteric infections in men who have sex with men. Curr Opin Infect Dis2018; 31(1): 50–56.
18.
McNeilCJKirkcaldyRDWorkowskiK. Enteric infections in men who have sex with men. Clin Infect Dis2022; 74(Suppl_2): S169–S178.
19.
RichardsonDPakianathanMEwensM, et al.The new 2023 BASHH sexually transmitted enteric infections guideline. Sex Transm Infect2023; 99(5): 363–364.
20.
SiddiqMO'FlanaganHRichardsonD, et al.Factors associated with sexually transmitted shigella in men who have sex with men: a systematic review. Sex Transm Infect2022; 99(1): 58–63.
21.
WahabNDubeyVSivachandranV, et al.Campylobacter spp. in men who have sex with men: a systematic review. Int J STD AIDS2024; 35(14): 1094–1102.
22.
DubeyVSivachandranVWahabN, et al.Giardia duodenalis in men who have sex with men: a systematic review. Frontline Gastroenterol2024; 15(5): 417–423.
23.
SivachandranVWahabNDubeyV, et al.Demographic, behavioural, and biological factors seen in men who have sex with men with Salmonella spp.: a systematic review. Venereology (Basel)2024; 3(4): 162–171.
24.
FitzpatrickCDohertySGeorgeS, et al.Hepatitis E in men who have sex with men: a systematic review. Frontline Gastroenterol2024; 15(6): 523–529.
25.
HughesRRichardsonDFitzpatrickC. Factors associated with Entamoeba histolytica proctocolitis in men who have sex with men: a systematic review. Frontline Gastroenterol2024; 15(4): 321–327.
26.
CharlesHProchazkaMThorleyK, et al.Outbreak of sexually transmitted, extensively drug-resistant Shigella sonnei in the UK, 2021-22: a descriptive epidemiological study. Lancet Infect Dis2022.
27.
BakerKSDallmanTJAshtonPM, et al.Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. Lancet Infect Dis2015; 15(8): 913–921.
28.
O'FlanaganHSiddiqMLlewellynC, et al.Antimicrobial resistance in sexually transmitted Shigella in men who have sex with men: a systematic review. Int J STD AIDS2023; 34(6): 374–384.
29.
MasonLCERichardsonDCharlesH, et al.Using demographics of patients to inform treatment of shigellosis in England. Lancet Microbe2024: 101026.
30.
RichardsonDPakianathanMEwensM, et al.The new 2023 BASHH sexually transmitted enteric infections guideline. Sex Transm Infect2023; 99(5): 363–364.
31.
MoolaSMunnZSearsK, et al.Conducting systematic reviews of association (etiology): the Joanna Briggs Institute's approach. Int J Evid Base Healthc2015; 13(3): 163–169.
32.
SimmsIGilbartVLByrneL, et al.Identification of verocytotoxin-producing Escherichia coli O117:H7 in men who have sex with men, England, November 2013 to August 2014. Euro Surveill2014; 19(43).
33.
HughesGSilalangPWereJ, et al.Prevalence and characteristics of gastrointestinal infections in men who have sex with men diagnosed with rectal chlamydia infection in the UK: an ‘unlinked anonymous’ cross-sectional study. Sex Transm Infect2018; 94(7): 518–521.
34.
ReinheimerCKepplerOTStephanC, et al.Elevated prevalence of multidrug-resistant gram-negative organisms in HIV positive men. BMC Infect Dis2017; 17(1): 206.
35.
WilliamsonDAChowEPFLeeD, et al.Risk factors for asymptomatic enteric pathogen detection among men who have sex with men. Open Forum Infect Dis2019; 6(9): ofz326.
36.
ChowEPFLeeDBondS, et al.Nonclassical pathogens as causative agents of proctitis in men who have sex with men. Open Forum Infect Dis2021; 8(7): ofab137.
37.
PurpuraLZuckerJLaSotaE, et al.Prevalence of gastrointestinal pathogens detected by multiplex polymerase chain reaction in a prospective cohort of men who have sex with men taking human immunodeficiency virus preexposure prophylaxis-New York city, 2019-2020. Open Forum Infect Dis2021; 8(8): ofab411.
38.
van BilsenWPHvan DulmEMatserA, et al.High carriage of ESBL-producing Enterobacteriaceae associated with sexual activity among men who have sex with men. Int J Antimicrob Agents2021; 57(3): 106276.
39.
VermaAHineAMJoelsonA, et al.The influence of hospitalization and HIV severity on gastrointestinal PCR panel evaluation of HIV-related acute diarrhea in New York City: a retrospective, cross-sectional study. Therap Adv Gastroenterol2022; 15: 17562848221092593.
40.
SurgersLChiarabiniTRoyerG, et al.Evidence of sexual transmission of extended-spectrum β-lactamase-producing enterobacterales: a cross-sectional and prospective study. Clin Infect Dis2022; 75(9): 1556–1564.
41.
MitchellHDWhitlockGZdravkovJ, et al.Prevalence and risk factors of bacterial enteric pathogens in men who have sex with men: a cross-sectional study at the UK's largest sexual health service. J Infect2023; 86(1): 33–40.
42.
de Korne-ElenbaasJvan der PuttenBCLBoekNDM, et al.Putative transmission of extended-spectrum β-lactamase-producing Escherichia coli among men who have sex with men in Amsterdam, The Netherlands. Int J Antimicrob Agents2023; 62(1): 106810.
43.
PhilipsbornRAhmedSMBrosiBJ, et al.Climatic drivers of diarrheagenic Escherichia coli incidence: a systematic review and meta-analysis. J Infect Dis2016; 214(1): 6–15.
44.
RichardsonDSavary-TrathenAFitzpatrickC, et al.Estimated prevalence and associations of sexually transmissible bacterial enteric pathogens in asymptomatic men who have sex with men: a systematic review and meta-analysis. Sex Transm Infect2024; 100(8): 532–537.
45.
PhanuphakNGulickRM. HIV treatment and prevention 2019: current standards of care. Curr Opin HIV AIDS2020; 15(1): 4–12.
46.
CresswellFVRossSBoothT, et al.Shigella flexneri: a cause of significant morbidity and associated with sexually transmitted infections in men who have sex with men. Sex Transm Dis2015; 42(6): 344.
47.
TraegerMWCornelisseVJAsselinJ, et al.Association of HIV preexposure prophylaxis with incidence of sexually transmitted infections among individuals at high risk of HIV infection. JAMA2019; 321(14): 1380–1390.
48.
GilbartVLSimmsIJenkinsC, et al.Sex, drugs and smart phone applications: findings from semistructured interviews with men who have sex with men diagnosed with Shigella flexneri 3a in England and Wales. Sex Transm Infect2015; 91(8): 598–602.
49.
McKayRA. Patient Zero: the absence of a patient’s view of the early North American AIDS epidemic. Bull Hist Med2014; 88(1): 161–194.
50.
RichardsonDNambiarKZNadarzynskiT. Understanding the diverse sexual repertoires of men who have sex with men, trans and gender-diverse groups is important for sexually transmitted infection prevention. BMJ Sex Reprod Health2021; 47(3): e3.
51.
OttawayZFinnertyFAmlaniA, et al.Men who have sex with men diagnosed with a sexually transmitted infection are significantly more likely to engage in sexualised drug use. Int J STD AIDS2017; 28(1): 91–93.
52.
DrücklerSvan RooijenMSde VriesHJC. Chemsex among men who have sex with men: a sexualized drug use survey among clients of the sexually transmitted infection outpatient clinic and users of a gay dating app in Amsterdam, The Netherlands. Sex Transm Dis2018; 45(5): 325–331.
53.
McGaugheyGRichardsonDVeraJ. Harm reduction services for people engaging in chemsex in Brighton, UK: a pilot qualitative study. Int J STD AIDS2023; 34(13): 940–944.
54.
RichardsonDDevlinJSmithH, et al.Sexually transmitted co-infections in men who have sex with men diagnosed with primary or secondary syphilis. J Eur Acad Dermatol Venereol2022; 36(6): e474–e475.
55.
RichardsonDSiddiqiAParasharK, et al.A pilot study evaluating antimicrobial antagonism in syphilis/Chlamydia trachomatis Co-infection in men who have sex with men. Eur J Ther2021; 27: 327–328.
56.
RabuszkoLChessellCLlewellynC, et al.Factors and presenting symptoms associated with intestinal spirochaetosis in men who have sex with men: a systematic review. J Eur Acad Dermatol Venereol2024; 38(4): 680–686.
57.
ChessellCRabuszkoLRichardsonD, et al.Factors associated with the sexual transmission of Strongyloides stercoralis in men who have sex with men: a systematic review. J Eur Acad Dermatol Venereol2024; 38(4): 673–679.
58.
LewisDA. New treatment options for Neisseria gonorrhoeae in the era of emerging antimicrobial resistance. Sex Health2019; 16(5): 449–456.
59.
KenyonCHerrmannBHughesG, et al.Management of asymptomatic sexually transmitted infections in Europe: towards a differentiated, evidence-based approach. Lancet Reg Health Eur2023; 34: 100743.
60.
RichardsonDPakianathanMEwensM, et al.British Association of Sexual Health and HIV (BASHH) United Kingdom national guideline for the management of sexually transmitted enteric infections 2023. Int J STD AIDS2023; 34(9): 588–602.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
