Original Studies

Increased Risk of Sexually Transmitted Infections in Men Who Have Sex With Men Taking Preexposure Prophylaxis: A Meta-analysis

Zhou, Qian PhD^∗,†; Liu, Jingwei PhD^∗,†; Li, Hao PhD^∗,†; Han, Yan PhD^∗,†; Yin, Yueping PhD^∗,†

From the ^∗Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College

^†STD Reference Laboratory, National Center for Sexually Transmitted Diseases Control, Chinese Center for Disease Control and Prevention, Nanjing, China

Acknowledgments: This work was supported by the National Science and Technology Major Project (2018ZX101010 01-004-003), CAMS Innovation Fund for Medical Sciences (2021-I2M-C&T-B-086), and the Nanjing Incubation Program for National Clinical Research Center (2019060001).

Conflict of Interest and Sources of Funding: The authors declare that there is no conflict of interest regarding the publication of this article.

Ethical Approval: Ethical approval was deemed not to be necessary as the data are publicly available literature.

Correspondence: Yan Han, PhD, Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing, China. E-mail: [email protected]; Yueping Yin, PhD, Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing, China. E-mail: [email protected].

Received for publication June 25, 2022, and accepted August 10, 2022.

Sexually Transmitted Diseases 49(11):p 733-739, November 2022. | DOI: 10.1097/OLQ.0000000000001698

Free

Up to 2 million new HIV infections occur yearly worldwide. Because there is no effective vaccine to prevent HIV transmission, behavioral and biomedical HIV prevention strategies are needed to reduce HIV acquisition.¹ Preexposure prophylaxis (PrEP) is an evidence-based way to prevent HIV infections for HIV-uninfected patients using antiretroviral medications. As a priority population for HIV prevention, there have been several large trials demonstrating the safety and efficacy of PrEP in reducing HIV transmission among men who have sex with men (MSM) who are at high risk for HIV transmission.² According to the results of a meta-analysis, the rate of HIV acquisition was reduced by 86% in MSM taking PrEP with high adherence.³

Although PrEP shows high efficacy in decreasing HIV incidence among these population, concerns remain that widespread PrEP uptake may result in behavioral change that leads to increases in sexually transmitted infections (STIs); one of the main reasons for this population taking PrEP is that it can effectively reduce their risk for acquiring an HIV infection without using condoms.³ Currently, increased incidence of chlamydia infection, gonorrhea, and syphilis in MSM has been reported in many countries.⁴ Also, the decreasing antibiotic susceptibility of Neisseria gonorrhoeae and the rise of more severe syphilis complications complicated the treatment and prognosis of STIs in high-risk populations for HIV/AIDS.^5,6

In this study, we performed a meta-analysis of the incidence density of STIs during the period of taking PrEP versus before taking PrEP in MSM, with the aim of investigating the possible increased risk of STIs among MSM taking PrEP, to provide data support for the STI prevention in PrEP participants.

METHODS

This meta-analysis was registered through PROSPERO (registration number CRD42022335974).

Search Strategy and Study Selection

The study was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.⁷ Two researchers (Q.Z. and J.L.) independently searched PubMed, EMBASE, Web of Science databases, China National Knowledge Infrastructure, and Wanfang Database from January 2012 (the year in which PrEP became available) to April 2022 using the terms ((chlamydia OR sexually) AND (prophy*) AND (HIV)) to identify relevant studies. Endnote X20 (Thomson Reuters, Toronto, Ontario, Canada) was used to manage the retrieved records, and RevMan 5.2 (RevMan 2014) was used to generate pictures of the flow diagram.

Two independent reviewers removed duplicates and screened literature based on the title and abstract, and then assessed the full texts of the remaining records. The studies for the meta-analysis were included if they fulfilled the following eligibility criteria: (1) published in English and Chinese, (2) focused on MSM, (3) used the PrEP intervention, and (4) reported the incidence density of STIs during PrEP period or before taking PrEP.

Data Extraction

We used a standardized form to summarize the data collected in the literature included. The data extracted included the following information: (1) title, first author, publication year, and research type; (2) study population, study location, and median age of the study population; (3) incidence data of syphilis, gonorrhea, and chlamydia infection; and (4) the population–time of observation after the intervention was conducted. Some of the data were in the supplementary files or discussion section, and we extracted this part of the data as well.

Assessment of the Quality

The quality was assessed according to the type of studies included. The quality of the nonrandomized studies was assessed by using the Methodological Index for Non-Randomized Studies (MINORS) scale.⁸ The MINORS scale for single-arm studies consisted of 8 items, including (1) a clearly stated aim, (2) inclusion of consecutive patients, (3) prospective collection of data, (4) end points appropriate to the aim of the study, (5) unbiased assessment of the study end point, (6) follow-up period appropriate to the aim of the study, (7) loss of follow-up less than 5%, and (8) prospective calculation of the study size. The items are scored 0 (not reported), 1 (reported but inadequate), or 2 (reported and adequate). The total score was 16, and trails with MINORS scores >12 were included in the study.⁹ For case-control studies or cohort studies, the Newcastle-Ottawa Scale (NOS) was used for quality assessment. The NOS tool assessed cohort studies in 3 areas: selection of study groups, comparability of the groups, and ascertainment of the outcome. The total score of NOS was 9 points.¹⁰

Meta-analysis

The heterogeneity was evaluated by the Higgins I² test statistic. If the value of I² was more than 50%, a random-effects model was applied; otherwise, a fixed-effects model was used. The incidence density was calculated by the number of incidences per 100 person-years (PY) for syphilis, gonorrhea, and chlamydia infection. The 95% confidence intervals (CIs) were determined from the incidences and PY assuming a Poisson distribution. To investigate the source of heterogeneity, subgroup analyses based on the type of research (prospective or retrospective study) and study location (North American or others) were conducted. Furthermore, the publication bias was detected by Egger's publication bias plot, and a P value less than 0.05 indicated a statistically significant publication bias.

RESULT

Literature Collection

A total of 714 records were identified from 3 databases published up to April 2022, of which 562 remained after duplicates had been removed. Of these, 511 were excluded because the title and abstract revealed them to be not related, non-English literature, reviews, books, case reports, and comments. The remaining 51 full-text articles were assessed for eligibility. Twenty-three of these studies did not provide data, and 8 provided only the combined incidence of STIs (Fig. 1). Finally, 20 studies met the inclusion criteria for the final analysis.^11–30 From these studies, we extracted 19 groups of incidence data of syphilis, 19 of gonorrhea, and 18 of chlamydia infection during the PrEP period. Five of these studies investigated the incidence data before taking PrEP.^{22,23,27–29}

Figure 1:
Flow diagram for selecting published studies for meta-analysis according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, generated by Review Manager Software (RevMan version 5.3).

Study Characteristics

Data extraction was performed on the 20 included articles, of which 6 were single-arm clinical trials, 9 were cohort studies, 2 were case-control studies, and 3 were retrospective descriptive studies. There were 9 studies from North America and 11 from other locations. A total of 8820 participants were enrolled in these studies, yielding a cumulative 10,563.75 PY of follow-up. The median age of the included population was 30 to 40 years. The characteristics and incidence data of these studies are summarized in Tables 1 and 2.

TABLE 1 - Characteristics of 20 Studies Included in the Meta-analysis

No.	First Author	Year	Type of Study	Study Location	Participants	Mid-Age, y
1	Zeggagh ¹¹	2022	Single-arm clinical Trial	France and Canada	429	35
2	Tabatabavakili ¹²	2022	Retrospective longitudinal cohort study	Canada	344	35
3	Saxton ¹³	2022	Single-arm clinical Trial	New Zealand	142	30
4	Mehta ¹⁴	2021	Prospective cohort study	Kenya	158	33
5	Jongen ¹⁵	2021	Prospective cohort study	Netherlands	571	39
6	De Baetselier ¹⁶	2021	Single-arm clinical Trial	Belgium	179	39
7	Chemtob ¹⁷	2021	Retrospective cohort study	Israeli	757	35
8	Azarnoosh ¹⁸	2021	Case-control study	Denmark	46	39
9	Ayerdi Aguirrebengoa ¹⁹	2021	Retrospective descriptive study	Spain	110	34.7
10	Van Praet ²⁰	2020	Single-arm clinical Trial	Belgium	131	40
11	Gravett ²¹	2020	Retrospective descriptive study	United States	81	32
12	Traeger ²²	2019	Single-arm clinical Trial	Australia	2981	34
13	Montaño ²³	2019	Retrospective cohort study	United States	365	30.6
14	John ²⁴	2019	Retrospective descriptive study	United States	104	32
15	Hoornenborg ²⁵	2019	Prospective cohort study	Netherlands	367	40
16	Tan ²⁶	2018	Single-arm clinical Trial	Canada	52	33
17	Nguyen ²⁷	2018	Prospective cohort study	Canada	109	36
18	Beymer ²⁸	2018	Case-control study	United States	275	35
19	Mayer ²⁹	2017	Prospective cohort study	United States	647	30
20	Marcus ³⁰	2016	Prospective cohort study	Canada	972	37.5

TABLE 2 - Incidence Data of 20 Studies Included in the Meta-analysis

Name of the Study	Syphilis		Chlamydia Infection		Gonorrhea
Name of the Study	Incidences	Population-Time	Incidences	Population-Time	Incidences	Population-Time
Zeggagh et al. ¹¹	112	864	275	864	261	864
Tabatabavakili et al. ¹²	15	282	102	282	139	282
Saxton et al. ¹³	14	133.25	71	133.25	98	133.25
Mehta et al. ¹⁴	—	—	39	145	—	—
Jongen et al. ¹⁵	116	994	519	1058	447	1058
De Baetselier et al. ¹⁶	22	268.5	101	268.5	93	268.5
Chemtob et al. ¹⁷	51	658.75	—	—	—	—
Azarnoosh et al. ¹⁸	5	23	14	23	14	23
Ayerdi Aguirrebengoa et al. ¹⁹	32	208	219	208	155	208
Van Praet et al. ²⁰	19	128.5	38	128.5	45	128.5
Gravett et al. ²¹	4	78.5	15	78.5	13	78.5
Traeger et al. ²²	252	3185	1242	3185	1434	3185
Montaño et al. ²³	25	365	135	365	165	365
John et al. ²⁴	3	58.25	13	58.25	10	58.25
Hoornenborg et al. ²⁵	75	681.75	186	681.75	180	681.75
Tan et al. ²⁶	4	48.75	16	48.75	16	48.75
Nguyen et al. ²⁷	16	109	31	109	44	109
Beymer et al. ²⁸	29	164.5	120	167.5	89	167.5
Mayer et al. ²⁹	62	1318	185	1318	241	1318
Marcus et al. ³⁰	56	850	177	850	203	850

Quality Assessment

The results of the quality assessment using the MINORS scale and NOS tool are presented in Tables 3 and 4. The methodological quality for 9 nonrandomized studies scored 12 to 16 using the MINORS scale. For 11 cohort studies and case-control studies, the NOS scores ranged from 7 to 9, which indicated a reliable quality.

TABLE 3 - The Score of 9 Nonrandomized Studies Using the MINORS Scale

No.	First Author	I	II	III	IV	V	VI	VII	VIII	Total
1	Zeggagh ¹¹	2	2	2	2	1	2	2	2	15
3	Saxton ¹³	2	2	2	2	1	2	1	2	14
6	De Baetselier ¹⁶	2	2	2	2	2	2	2	2	16
9	Ayerdi Aguirrebengoa ¹⁹	2	2	0	2	2	2	2	0	12
10	Van Praet ²⁰	2	2	2	1	2	2	2	2	15
11	Gravett ²¹	2	2	0	2	2	2	2	0	12
12	Traeger ²²	2	2	2	2	2	2	2	2	16
14	John ²⁴	2	2	0	2	2	2	2	0	12

Numbers I to VIII in the heading signified the following: I, a clearly stated aim; II, inclusion of consecutive patients; III, prospective collection of data; IV, end points appropriate to the aim of the study; V, unbiased assessment of the study end point; VI, follow-up period appropriate to the aim of the study; VII, loss of follow-up less than 5%; VIII, prospective calculation of the study size. The items are scored 0 (not reported), 1 (reported but inadequate) or 2 (reported and adequate).

TABLE 4 - The Score of 11 Cohort Studies and Case-Control Studies Using the NOS Tool

No.	First Author	I	II	III	IV	V	VI	VII	VIII	Total
2	Tabatabavakili ¹²	1	1	1	0	2	1	1	1	8
4	Mehta ¹⁴	1	1	1	1	2	1	1	1	9
5	Jongen ¹⁵	1	1	1	1	2	1	1	1	9
7	Chemtob ¹⁷	1	1	1	1	2	0	1	1	8
8	Azarnoosh ¹⁸	1	1	1	0	2	1	0	1	7
13	Montaño ²³	1	1	1	0	2	1	1	1	8
15	Hoornenborg ²⁵	1	1	1	1	2	1	1	1	9
16	Tan ²⁶	1	1	1	1	2	1	1	0	8
17	Nguyen ²⁷	1	1	1	1	2	0	1	0	7
18	Beymer ²⁸	1	1	0	1	2	1	1	1	8
19	Mayer ²⁹	1	1	1	1	2	1	1	1	9
20	Marcus ³⁰	1	1	1	1	2	0	1	1	8

Numbers I to VIII in the heading signified the following: I, representativeness of the exposed cohort; II, selection of the nonexposed cohort; III, ascertainment of exposure; IV, demonstration that outcome of interest was not present at start of study; V, compare ability of cohorts on the basis of the design or analysis; VI, assessment of outcome; VII, was follow-up long enough for outcomes to occur; VIII, adequacy of follow-up of cohorts (1 point for each item, 2 points for compare ability, 9 points in total).

Meta-analysis

After pooling the incidence density for the 3 pathogens during the PrEP period, the pooled estimate of incidence density of syphilis was 9.53 per 100 PY (95% CI, 8.21–11.06), whereas it was 36.48 per 100 PY (95% CI, 31.47–42.28) for chlamydial infection and 34.79 per 100 PY (95% CI, 29.50–41.02) for gonorrhea (Fig. 2). The pooled estimate of incidence density of syphilis before taking PrEP was 5.95 per 100 PY (95% CI, 4.59–7.71), whereas it was 20.66 per 100 PY (95% CI, 17.44–24.49) for chlamydial infection and 19.52 per 100 PY (95% CI, 16.91–22.53) for gonorrhea. After performing the Wilcoxon rank sum test, the incidence density of 3 STIs during the PrEP period was significantly lower than the value during PrEP (P < 0.05).

Figure 2:
A, Pooled incidence density of syphilis. B, Pooled incidence density of chlamydial infection. C, Pooled incidence density of gonorrhea.

Subgroup Analysis

Subgroup analysis was performed according to prospective or retrospective studies. For prospective studies, syphilis, chlamydial infection, and gonorrhea incidence densities were 9.61, 34.34, and 30.77 per 100 PY, respectively, compared with 9.25, 40.46, and 42.87 per 100 PY for retrospective studies (Fig. 3). Syphilis, chlamydial infection, and gonorrhea incidence densities were 7.50, 30.08, and 28.18 per 100 PY for studies in North America, respectively, and these data were 11.33, 43.82, and 41.91 per 100 PY for studies in other regions (Fig. 4).

Figure 4:
A, Syphilis incidence density by study location subgroup analysis. B, Chlamydial infection incidence density by study location subgroup analysis. C, Gonorrhea incidence density by study location subgroup analysis.

Publishing Bias

Publication bias testing of the included studies was conducted using Egger's method. Egger's test results (P_syphilis = 0.536 > 0.05; P_chlamydial = 0.235 > 0.05; P_gonorrhea = 0.714 > 0.05) showed no publication bias for any of the 3 pathogens (Fig. 5).

Figure 5:
A, Egger's publication bias plot of syphilis. B, Egger's publication bias plot of chlamydial infection. C, Egger's publication bias plot of gonorrhea.

DISCUSSION

As an effective method to prevent HIV infection in high-risk populations, PrEP is gradually being studied more and more in MSM.³¹ Meanwhile, for those studies using PrEP, STI testing is required every 3 months for syphilis, chlamydia, and gonorrhea, which provides us with the feasibility to investigate the incidence density of the 3 pathogens.³² Because incidence density measures the occurrence of disease onsets in a population per unit of time of follow-up, it could be a better indicator of the occurrence of STIs in MSM during the PrEP period than prevalence, which referred to all cases in the population at a given time. This meta-analysis aimed to generate estimates for incidence density for 3 STIs among MSM taking PrEP. Pooled data from 20 studies showed that the incidence density of syphilis was 9.53 per 100 PY, whereas it was 36.48 per 100 PY for chlamydial infection and 34.79 per 100 PY for gonorrhea. The combined incidence density of these 3 STIs was 81.07 per 100 PY.

After performing a comparison of the incidence density during the PrEP period with that before taking PrEP, we found that the former was significantly higher than the latter. Comparing the pooled data from MSM using PrEP with other MSM not using PrEP on the incidence of STI in MSM after 2016, for syphilis incidence density, in a Thai study, the incidence density of syphilis in MSM was 4.5 per 100 PY,³³ whereas in another Chinese study, the incidence density of syphilis was 5.6 per 100 PY³⁴; the syphilis incidence density in MSM using PrEP in this study was higher than the results in MSM not using PrEP. As for the incidence density of gonorrhea and chlamydia infection, the study showed that the incidence of gonorrhea in MSM was 15.6 to 21.1 per 100 PY, and chlamydia infection was 19.3 to 19.5 per 100 PY.^27,35 Some studies provided the combined incidence density of gonorrhea and chlamydia infection of 18.0 to 33.1 per 100 PY,^36,37 which was lower than the results of our study. Men who have sex with men taking PrEP have high incidence of STIs, which may be due to these factors: that PrEP helps to reduce the acquisition of HIV may increase more high-risk sexual behaviors in MSM such as multiple sexual partners, the decrease in condom use, and more frequent and more vigorous sexual activity.^22,38 Loss to follow-up bias could not be negligible. Moreover, all the studies included in this meta-analysis had a loss of follow-up rate of less than 10%. Those who were knowingly exposed to STIs or symptomatic were more likely to finish follow-up, which would also increase the statistical incidence density of STIs.

The results of subgroups analysis indicated the differences by study type and study location. In the study type subgroup analysis, it was found that the incidence density tended to be lower in prospective studies than in retrospective studies, possibly because of limitations in using data from trials or cohort studies to estimate STI incidence and because some studies were not specifically designed to assess STI incidence.³⁹ In the study location subgroup analysis, incidence density was lower in North America than in other regions, and there may be multiple influences, including changes in sexual behavior among MSM and mobility of the MSM population.^40–42

Considering the progressive increase in antibiotic resistance of sexually transmitted disease pathogens and more complex treatment of STIs in recent years, the high incidence of STIs in MSM population taking PrEP is a cause for alarm. As can be surmised from the higher STI incidence results in this study, sustained efforts to control the transmission of STIs among PrEP users and their sexual partners would be meaningful. Examples include education of this population and emphasis on condom use during sexual behavior. Also, as part of the PrEP program, routine testing and comprehensive treatment of STIs (including syphilis, chlamydia infection, and gonorrhea) are highly prevalent among MSM. Further research to evaluate new biomedical strategies also needs to be conducted for the prevention of bacterial STIs, such as antibiotic PrEP and antibiotic use in postexposure prophylaxis.⁴³

Through this meta-analysis and systematic review, we estimated the incidence density of 3 STIs in an MSM population taking PrEP. The high incidence of STIs in the MSM taking PrEP needs to be increasingly appreciated, and the prevention of STIs is valuable among MSM alongside HIV prevention uptake.

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Increased Risk of Sexually Transmitted Infections in Men Who Have Sex With Men Taking Preexposure Prophylaxis: A Meta-analysis

Background

Methods

Results

Conclusions