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Globally, men who have sex with men MSM are disproportionately burdened with syphilis. This review describes the published literature on trends in syphilis infections among MSM in the US and Western Europe from , the period with the fewest syphilis infections in both geographical areas, onwards.

We also describe disparities in syphilis trends among various sub-populations of MSM. Taken together, our findings indicate an increase in the s and rates per , of syphilis infections among MSM in the US and Western Europe since Editor: Viviane D.

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability: This is a systematic review of existing and available syphilis trend studies conducted in the US and Western Europe.

The article selection criteria are included in the methods and the articles included in this review can be reproduced using the key words. Competing interests: The authors have declared that no competing interests exist. Globally, men who have sex with men MSM for a disproportionate burden of syphilis infections [ 1 — 3 ]. In Western Europe, MSM also for the majority of primary and secondary syphilis cases and remain the group most at risk for contracting syphilis [ 3 ].

Primary and secondary syphilis are the most infectious stages of syphilis [ 4 ]. Syphilis causes inflammatory genital ulcers and lesions which can increase the risk of HIV transmission by increasing HIV shedding, and acquisition by providing a portal of entry to the HIV virus [ 5 ]. Syphilis also complicates the clinical course of HIV by increasing viral load [ 5 , 6 ]. It has also been associated with a higher rate of treatment failure in HIV-infected persons [ 7 ].

However, around , intermittent outbreaks of syphilis were reported in many urban areas in the US and Western Europe [ 8 — 13 ]. These outbreaks occurred almost exclusively among MSM and were attributed to increases in risky sexual behaviors such as condomless anal sex CAS , exchange sex, illicit drug use before sex, multiple sexual partners, and high-risk anonymous sexual contacts [ 14 ].

Syphilis outbreaks continue to occur sporadically in the US and Western Europe [ 3 ]. Given the continued risk of syphilis transmission, its close association with HIV infection, and the disproportionate disease burden among MSM in the US and Western Europe, there is a need to examine and understand syphilis trends among MSM in both geographic areas.

The purpose of this systematic review is to descriptively examine and compare recent trends over time in syphilis cases among MSM in the US and Western Europe. This review will also describe disparities in syphilis trends by HIV status, race, and age among MSM with the aim of identifying sub-groups that would benefit from enhanced syphilis screening and intervention strategies in the US and Western Europe. The current review focuses on syphilis data from , the year record lows in the rate of syphilis cases in the US and Western Europe were reported, and afterwards [ 9 , 15 ].

A systematic literature search was conducted to find research papers and surveillance reports that assessed changes over time — in sexual risk behaviors and the prevalence of sexually transmitted infections STI among MSM. Articles for inclusion in this review were further limited to studies and surveillance reports that met the following criteria: reported on MSM who resided in the US or Western Europe; reported on syphilis primary, secondary, and latent cases at multiple time points with dates of onset, diagnosis, or official notification to a public health authority from to ; reported in full length peer-reviewed publication abstracts, posters, books, and dissertations were excluded ; and published in English from January to June In summary, for this review, we limited eligible articles to peer-reviewed studies and surveillance reports on syphilis trend data on MSM in the US and Western Europe that commenced from or afterwards, and were published in English between and Eligible studies were limited to those published between and in order to review recently published studies and minimize the inclusion of multiple studies with syphilis trends data over the same time period.

Modeling studies, intervention studies, systematic reviews, and meta-analyses were excluded. We did not include data that was obtained exclusively from institutionalized populations and very high-risk populations such as sex workers because data from these populations may influence the interpretation of our findings.

Data were coded for location of residence of cases country and city , time frame i. We extracted syphilis trend data commencing in or later from all studies and reports. If an article presented unduplicated syphilis trend data from more than one city or country separately, we presented trend data from these cities or countries separately in the tables and graphs, otherwise aggregate were presented. A two-tailed level of ificance value of 0.

Data were extracted independently and then reviewed by two people to ensure their accuracy. This systematic review and the methodological evaluation of each study were written up according to the PRISMA standard a protocol used to evaluate systematic reviews S1 Checklist [ 17 ]. Fig 1 is a flow diagram showing the article screening process. The initial search resulted in 7, citations. After removing duplicates, there were 7, citations to review for inclusion. Of these, 6, citations did not meet the inclusion criteria and citations were retained for retrieval of the full-length article.

Review of the full-length articles yielded 39 articles that met the inclusion criteria. If multiple articles reported on overlapping data sources or time points, the most recent or most comprehensive article larger sample size, more time points, trend data showing disparities by HIV status, race, or age, etc. Through this process, 16 articles were excluded because they contained duplicate data and outcomes. An additional five articles were excluded because the data were specific to a very high-risk sub-population i.

A final list of 18 articles was used to describe overall syphilis trends for this systematic review. These 18 articles 10 from the US and 8 from Western Europe included data from independent convenience samples and case surveillance reports from different cities and countries that were considered in this paper to be 24 unduplicated studies. Of the 18 articles 24 studies that met the inclusion criteria, 10 articles 12 studies reported overall syphilis trends among MSM who lived in the US [ 18 — 27 ] and 8 articles 12 studies reported overall syphilis trends among MSM who lived in Western Europe [ 28 — 35 ].

One article from the US included syphilis trend data from three different cities [ 25 ], resulting in 12 studies from 10 articles. Similarly, one article from Western Europe included syphilis trend data from five different countries in Western Europe [ 32 ], resulting in 12 studies from 8 articles.

Table 1 presents a summary of the syphilis trend studies in the US; Table 2 presents a summary of syphilis trend studies in Western Europe. Among the trend studies conducted in the US, four were conducted in California [ 18 — 21 ]; one each was conducted in Alabama [ 22 ], Washington [ 23 ], and Wisconsin [ 24 ]; one study obtained data from three cities New York City, Miami, and Philadelphia [ 25 ]; one study obtained syphilis case report data from 27 states [ 26 ]; and another study utilized syphilis case surveillance data from every state and the District of Columbia that were reported to the CDC [ 27 ].

Case surveillance data were used to analyze syphilis trends for all the studies conducted in the US [ 18 — 27 ]. Two studies conducted tests of ificance to determine if syphilis case data changed ificantly over time [ 25 , 26 ]. The most common measure used in determining syphilis trends was the of reported syphilis cases—ten studies evaluated the of reported syphilis cases over time and two studies reported syphilis case rates.

For the two studies that estimated rates, denominators were obtained from US census data and published reports [ 23 ] and from the National Center for Health Statistics [ 26 ]. Of the 12 studies that reported overall syphilis trends, 11 reported on trends in infectious syphilis primary and secondary syphilis and one reported on trends in primary, secondary, and early latent syphilis Table 1.

Of the 12 studies conducted in Western Europe see Table 2 , one each was conducted in England and Wales [ 28 ], England [ 29 ], and Scotland [ 30 ]. Two studies used data from Ireland 31, 32 while the other studies were each conducted in France [ 32 ], Sweden [ 32 ], Greece [ 32 ], the Netherlands [ 32 ], Norway [ 33 ], Denmark [ 34 ], and Germany [ 35 ]. One surveillance report presented comprehensive syphilis surveillance trends among MSM from eight Western European countries [ 32 ].

From this comprehensive syphilis surveillance report, we included non-duplicate data from five countries—Ireland, France, Sweden, Greece, and the Netherlands. We excluded data from the other two countries because they duplicated data from studies already included in our review or were not as comprehensive. For 11 of the 12 studies from Western Europe, the investigators obtained data from syphilis case surveillance systems and used the of syphilis cases to assess syphilis trends [ 28 — 30 , 32 — 35 ]. Among the three studies that reported syphilis case rates, denominators were obtained from general population surveys and census population estimates for MSM [ 31 ], a national database of MSM with current HIV diagnoses [ 29 ], and the of syphilis tests among MSM in a national surveillance system [ 36 ].

Two studies reported trends in infectious syphilis only, four reported on primary, secondary, and early latent syphilis, and six reported on syphilis diagnoses no stage specified Table 2. Of the 21 countries in Western Europe, nine countries in Western Europe consistently collect syphilis surveillance data on MSM [ 32 , 35 ].

This review included data from eight of these countries in Western Europe that met our inclusion criteria. Overall, we included both national surveillance report national data and localized study data from smaller geographical areas in the US and Western Europe because national surveillance data tended to report only overall syphilis trends while localized study data tended to report disparities HIV, race, and age in syphilis trends in addition to overall trends.

Overall, the data from the studies conducted in the US document an increase in syphilis cases over time Fig 2. Among most studies that commenced data collection between and , syphilis cases were at their lowest during this period, but showed an increase from and beyond.

Six studies reported a consistent increase upward trend without a decline at any time point over the period for which data were available [ 19 — 21 , 25 — 27 ]. Gunn and colleagues examined syphilis cases among MSM in San Diego between and and reported a consistent increase [ 21 ]. The of syphilis cases among MSM in the Gunn et al. Chew and colleagues also reported a consistent increase in the of syphilis cases among MSM in California between and [ 19 ].

Su et al. Peterman and colleagues used national syphilis case data that was reported to the CDC from all states and the District of Columbia to examine syphilis trends and reported a consistent increase in syphilis cases among MSM from approximately 6, cases in to 14, cases in [ 27 ]. Four studies reported an overall increase in syphilis over time, despite intermittent periods of declining reported syphilis diagnoses [ 18 , 22 — 24 ].

Kerani et al. Syphilis diagnoses remained stable between and , and consistently increased from approximately 45 in to diagnoses in [ 23 ]. Hook and colleagues assessed syphilis trends between and among MSM in Jefferson County, Alabama [ 22 ].

They documented an overall increase in syphilis cases during the study period, increasing from less than 5 cases in to greater than 60 cases in Two studies conducted tests of ificance of syphilis trends [ 25 , 26 ]. Brewer et al. The of syphilis cases ificantly increased from 20 cases in to cases in in New York City; 29 cases in to cases in in Miami-Fort Lauderdale; and from 2 cases in to 70 cases in in Philadelphia.

Overall, as Fig 2 demonstrates, syphilis cases among MSM in the US have increased from their lowest prevalence in in a of diverse geographic settings. Kerani and colleagues used surveillance data from King County, Washington, to compare trends in the rate of primary and secondary syphilis among MSM by HIV status [ 23 ]. Biedrzycki and colleagues used surveillance data between and from the Wisconsin Department of Public Health to investigate the relationship between syphilis trends and HIV infection among young Black MSM in Milwaukee County, Wisconsin [ 24 ].

The authors observed that an increase in syphilis cases was indicative of increased risk behaviors and high-risk sexual networks of young Black MSM in Milwaukee County, and hypothesized that these factors also likely facilitated an increase in HIV cases in this population. In summary, data from these two studies suggest that the increases in syphilis trends may be more pronounced among HIV-positive MSM and that increased syphilis transmission may be accompanied by increased HIV transmission among MSM and vice versa.

This systematic review also evaluated racial differences in syphilis trends Table 1. Their findings showed racial differences in syphilis trends over time. By , the syphilis prevalence among API MSM was estimated at cases per , compared to approximately cases per , among White MSM, despite the similar rates for these two groups in [ 37 ].

Su and colleagues used syphilis case reports from 27 states to examine racial disparities in syphilis trends among Black, Hispanic, and White MSM between and [ 26 ]. Their study findings showed ificant disparities in syphilis trends.

Their study concluded that there was an overall increase in syphilis cases among Black MSM in San Francisco during the study period despite intermittent periods of decline in syphilis cases [ 38 ]. Finally, Patton and colleagues used surveillance data from 34 states and the District of Columbia to determine racial differences in syphilis trends among MSM between and [ 2 ]. Overall the proportion of primary and secondary cases attributed to MSM increased from There was a We examined syphilis trends by age among MSM.

Consistent with these findings, Su and colleagues, using data from 27 states, observed that the greatest absolute increase in syphilis rates between and occurred among MSM between 20 and 24 years and MSM between 25 and 29 years of age [ 26 ]. Lastly, Patton and colleagues examined data from to from MSM in 34 states and the District of Columbia and showed that the greatest percentage increases by age group occurred among MSM aged between 25 and 29 years Fig 3 illustrates trends in reported syphilis cases among MSM in Western Europe from for the studies and surveillance reports included in this review.

In all the studies, syphilis cases among MSM in Western Europe were lowest between and and have increased since. Two studies presenting syphilis surveillance data from Greece and Germany showed a consistent increase in syphilis cases [ 35 ]. National surveillance data from Germany showed a consistent increase in syphilis cases among MSM, increasing from approximately cases in to cases in while national surveillance data from Greece showed an increase from 47 cases in to cases in [ 35 ]. The remaining studies showed an overall increase despite intermittent periods of decline [ 28 ].

Malek et al reported an increase in the of syphilis diagnosis among MSM in England from syphilis cases in to cases in [ 29 ]. Using surveillance data, Jebbari et al reported an increase in the of syphilis cases among MSM in England and Wales from cases in to cases in [ 28 ]. In France, national case surveillance data show an increase in the of syphilis cases among MSM from 30 cases in to cases in [ 32 ].

Hopkins and colleagues reported an increase in syphilis case rates from 5. Another study conducted in Sweden demonstrated an increase in the of syphilis cases among MSM from 42 cases in to approximately cases in [ 32 ]. Potts and colleagues examined syphilis trend data among MSM in Scotland from to [ 30 ]. Their study findings showed an uneven syphilis trend during the study period. There was a consistent increase in national syphilis cases in Scotland between and , followed by a decline in cases and , then a steady increase in and , and a decline in Finally, an analysis of national surveillance data from the Netherlands also demonstrated an overall increase in syphilis cases among MSM from approximately cases to greater than cases between and [ 32 , 34 ].

Hopkins et al. Syphilis rates increased from 0 per , in to 1, per , in among HIV-positive MSM in this study. The authors found that between and , the odds of being diagnosed with syphilis increased ificantly from 2.

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