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International Journal of Infectious Diseases 17 (2013) e84–e92

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International Journal of Infectious Diseases


journal homepage: www.elsevier.com/locate/ijid

Review

Syphilis in the most at-risk populations in Latin America and the Caribbean:
a systematic review
Ana Clara Zoni, Mónica Alonso González *, Helena Werin Sjögren
HIV/STI Project, Family and Community Health Area, Pan American Health Organization, 525 Twenty-third Street, NW, Washington, DC 20037, USA

A R T I C L E I N F O S U M M A R Y

Article history: Objective: To describe syphilis prevalence in men who have sex with men (MSM), the transgender
Received 18 February 2012 population, and sex workers and their clients, identifying critical geographical areas, trends, and data
Received in revised form 21 May 2012 gaps in Latin America and the Caribbean.
Accepted 2 July 2012
Methods: A systematic review of syphilis prevalence was conducted by searching PubMed, LILACS,
Corresponding Editor: William Cameron, EMBASE, conference records, and other sources (2000–2010).
Ottawa, Canada
Results: Forty-eight articles were included in the review, from which 84 data points were identified
relating to MSM and female sex workers and only 10 relating to the transgender population, male sex
Keywords: workers, and clients of sex workers. Most studies were from Latin America (83%), with fewer from the
Syphilis Caribbean (17%). Critical ‘hotspot’ cities were Sao Paulo, Buenos Aires, Guatemala, Puerto Barrios, San
Most at-risk population José, San Pedro, Managua, San Salvador, and Acajutla, with high syphilis prevalence in more than one
Prevalence
study population. Gaps in the availability of information on syphilis prevalence were identified for
Infectious diseases
Ecuador, Uruguay, and Bolivia, and most countries in the Caribbean. Chronological trends showed that
syphilis infection is well-established among the study populations.
Conclusions: Consistently high levels of syphilis among the investigated populations throughout the
study period show that there is a need to improve monitoring, surveillance, and evaluation of sexually
transmitted infection control interventions among these populations. Improved reporting and
standardization of syphilis testing is recommended, as well as a heightened focus on more effective
syphilis control strategies.
ß 2012 International Society for Infectious Diseases. Published by Elsevier Ltd. Open access under CC BY-NC
-ND license.

Despite syphilis being a treatable disease, diagnostic challenges


1. Introduction
continue to affect global control efforts, due to the natural history
of the disease (a long latent infection stage) and testing algorithms
Syphilis is an important public health problem worldwide,
that need to be interpreted in the context of clinical history,
having serious consequences for health if left untreated. During the
examination, and any past record of treatment. Given the various
early phases of infection, common symptoms include the
clinical manifestations of syphilis, laboratory testing is a very
appearance of a sore called a ‘chancre’ at the site of inoculation,
important aspect of diagnosis. Syphilis should be diagnosed using a
followed by headache, achiness, and a rash. Even without
combination of treponemal and non-treponemal serological tests
treatment, both primary and secondary lesions resolve, and the
to reach a high sensitivity and specificity, for both asymptomatic
infection then enters a latent stage. The disease may also progress
and symptomatic infections. The use of non-treponemal tests
to a number of significant late manifestations (tertiary syphilis),
alone is not advised because of the delay in the production of
including cardiovascular, gummatous, and neurological complica-
antibodies in the early stages, the incidence of false-positives, and
tions. Mother-to-child transmission may occur at any stage of
the prozone phenomenon. Quantitative non-treponemal tests are
pregnancy in infected women and can trigger abortion, fetal death,
particularly useful for monitoring the response to treatment, to
neonatal mortality, premature labor, low birth weight, and
estimate the stage of disease, to distinguish active syphilis from
congenital syphilis.1 In addition, syphilis is one of a number of
lifetime syphilis (titers of 8 or more dilutions are interpreted as
ulcerative diseases that increase the risk of acquisition and
corresponding to active infection), and in the diagnosis of re-
transmission of HIV through several mechanisms.2
infection (because treponemal tests remain positive for life).
Treponemal tests are more specific, become positive earlier, and
* Corresponding author. Tel.: +1 202 9743954; fax: +1 202 9743631. are more perdurable than the above-mentioned tests, but titers do
E-mail address: alonsomon@paho.org (M.A. González). not correlate with the activity of the infection.1

1201-9712 ß 2012 International Society for Infectious Diseases. Published by Elsevier Ltd. Open access under CC BY-NC-ND license.
http://dx.doi.org/10.1016/j.ijid.2012.07.021
A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92 e85

According to recent World Health Organization (WHO) these groups were condensed into two: (1) prevalence of active
estimates, in 2008 there were 10 million new cases of syphilis syphilis tested, this included quantitative non-treponemal test or
among adults around the world, and 2.8 million (28%) occurred in non-treponemal plus treponemal tests; (2) prevalence of unspeci-
America.3 Estimated values for syphilis prevalence for the year fied syphilis tested for those studies that did not distinguish
2005 in male and female adults of the general population in this between active or lifetime syphilis, or those that did not report the
region were 1.27% and 1.22%, respectively.4 Countries of Latin test algorithm applied. Clinical signs and symptoms were not used
America and the Caribbean (LAC) are making efforts to control to adjust the abovementioned categories given that they were
syphilis infection, and in particular are aiming to eliminate inconsistently and rarely reported.
congenital syphilis.3,5 Statistical trend testing was analyzed where possible.
Syphilis is not homogeneously spread within the population;
the most at-risk populations (MARPs) (and subgroups within
3. Results
these), such as men who have sex with men (MSM), transgender
(TG), and sex workers (SW) and their clients (CSW), are
The initial search identified a total of 536 citations. Most studies
disproportionately affected by syphilis.3,6 An overview of syphilis
were excluded at first screening because they did not report
levels in the region would give a better understanding of the
syphilis prevalence, or were conducted in countries outside of LAC,
epidemiological situation of syphilis in MARPs, and help to
leaving 242 studies for further screening. Of these, 194 were
strengthen response plans and strategies and the achievement
excluded, the majority because they addressed other population
of national, regional, and global targets, including the Initiative for
groups. Agreement between reviewers was unanimous for the
Elimination of Mother-to-Child Transmission of HIV and Congeni-
excluded citations. Figure 1 shows the search algorithm used,
tal Syphilis (EI), United Nations General Assembly Special Session
which was organized in accordance with the PRISMA guidelines.
(UNGASS) targets, and Millennium Development Goals.
Forty-eight full-text articles met the inclusion criteria and these
The objective of this study was to describe the prevalence of
provided 95 data points (Table 18–55). Study population totals are
syphilis in MSM, TG, SW, and CSW, identifying critical geographical
given in Table 2.
areas, trends, and data gaps in the countries of LAC.
Studies on the prevalence of syphilis in the populations under
investigation were identified for only 18 of the 45 countries and
2. Methods
territories of LAC; 83% of the studies were reported from Latin
American and 17% from the Caribbean.
A systematic review was conducted in order to find data on
syphilis prevalence in MSM, TG, SW, and CSW in LAC. Potentially
relevant abstracts were identified in the PubMed, LILACS, and
EMBASE databases. Experts on the topic were consulted and 536 citaons idenfied (all populaon groups)
institutional web pages were also reviewed. The following search 287 from PubMed
terms were used: ‘‘Syphilis’’ OR ‘‘Treponema pallidum’’ AND 106 from LILACS
92 from EMBASE
‘‘Prevalence’’ AND a combination of the names of all countries, 51 idenfied through other sources (including gray literature)
capitals, and main cities of LAC. Keywords were introduced in the
database as text terms (all fields). Detailed information on the 155 citaons removed
search terms and sources is provided as Supplementary Material, 45 conducted in other countries
110 without the outcome of interest
available online. (syphilis prevalence)
This review was conducted and reported in accordance with the
PRISMA (Preferred Reporting Items for Systematic Reviews and 139 duplicates removed
Meta-Analyses) Statement issued in 2009.7
For inclusion in the review, studies had to fulfill the following
242 citaons screened
criteria: (1) published and unpublished studies from 2000 to 2010
that provided syphilis prevalence in adults or adolescents among
the following population groups: MSM, TG, SW, and CSW, within 194 full-text citaons excluded with reasons
LAC countries; (2) sample size of at least 100 participants for all 156 did not meet populaon group criteria
(general populaon, pregnant women,
groups, except for the TG population for which the minimum prisoners, drug users…)
sample size was lowered to 75. 25 did not meet other inclusion criteria (low
sample size or other age group (congenital
Two reviewers independently applied the inclusion criteria to
syphilis studies)
potential studies, with any disagreements resolved by discussion. 6 case studies
For abstracts that met the inclusion criteria, the full papers were 3 reviews without new data to include
2 cost-effecveness studies
assessed. The principal outcome of this study was the syphilis 1 sensivity/specificity study
prevalence in at least one of the populations under analysis. Data 1 case–control study
were registered based on syphilis prevalence per location,
vulnerable group, and year. Thus, one citation could yield more
48 full text citaons included
than one record.
The syphilis test algorithms were organized into the following
categories: (1) non-treponemal test (a positive rapid plasma reagin
(RPR) or venereal disease research laboratory (VDRL) test), (2) 95 records included in database
treponemal test (a positive Treponema pallidum hemagglutination SW: 53 MSM: 35
CSW: 2 TG: 5
assay (TPHA), fluorescent treponemal antibody-absorption (FTA-
ABS) test, or Treponema pallidum particle agglutination (TPPA)
test), (3) quantitative non-treponemal test (a positive RPR or VDRL SW: sex worker; MSM: men who have sex with men; CSW: clients of sex workers;
with a titer 1:8), (4) non-treponemal and treponemal tests
TG: transgender.
(positive RPR or VDRL with a confirmatory TPHA, FTA-ABS test, or
TPPA test), and (5) unknown testing algorithm. For the analysis, Figure 1. Search algorithm organized according to PRISMA guidelines.
e86
Table 1
Characteristics of records included in the systematic reviewa

Author (publication date) Country Sub-area/city Enrollment Type of sampling Test algorithm Sample % Prevalence
date (setting) size (95% CI)

Men who have sex with men


Benzaken et al. (unpublished)8 Brazil Manaus 2008 RDS Trep 824 4 (2.6–5.8)
Cáceres et al. (2008)9 Peru Lima, Chiclayo, Trujillo 2001 Cluster (MV) Non-trep and Trep 166 28.9
Clark et al. (2008)10 Peru Lima 2007 Convenience Non-trep and Trep 559 10.0
(STI clinic)
COPRESIDA (2009)11 Dominican Santiago 2008 RDS Non-trep Q 327 8.7
Republic
Barahona 2008 RDS Non-trep Q 281 6.9
La Altagracia 2008 RDS Non-trep Q 270 6.8
Santo Domingo 2008 RDS Non-trep Q 509 6.1
Figueroa et al. (2008)12 Jamaica Unknown 2007 Unknown Unknown 201 5.5
Lahuerta et al. (2011)13 Guatemala Escuintla 2009 SS (STI clinic) Non-trep and Trep 144 1.4

A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92


Convenience Non-trep and Trep 385 0.0
(mobile van)
Lama et al. (2010)14 Peru Lima, Sullana, Piura, Arequipa, 2003 Targeted (MV) Non-trep and Trep 2703 3.4
Iquitos, Pucallpa
Lignani et al. (2000)15 Brazil Belo Horizonte 1999 Unknown Unknown 279 10.6
Ministry of Health, Nicaragua (2003)16 Nicaragua Managua, Bluefields, Corinto 2002 TLS (MV) Non-trep and Trep 162 10.5
Ministry of Health, Honduras (2008)17 Honduras San Pedro 2006 RDS Non-trep and Trep 210 11.3 (4.8–20.2)
La Ceiba 2006 RDS Non-trep and Trep 213 0.3 (0.0–0.6)
Tegucigalpa 2006 RDSb Non-trep and Trep 204 4.4 (1.8–8.8)
Ministry of Health, El Salvador (2009)18 El Salvador San Miguel 2008 RDS Non-trep and Trep 174 0.7 (0.0–1.7)
San Salvador 2008 RDS Non-trep and Trep 516 6.3 (6.0–8.9)
Ministry of Health, Nicaragua (2010)19 Nicaragua Chinandega 2009 RDS Unknown (active) 286 3.1
Managua 2009 RDS Unknown (active) 577 6.4
20
PAHO (unpublished) Paraguay Unknown Unknown Unknown Unknown 115 10.0
Pando et al. (2006)21 Argentina Buenos Aires 2001 Convenience (MV) Non-trep and Trep 694 16.9 (14.1–20.0)
Pando et al. (2009)22 Argentina Buenos Aires 2008 RDS Non-trep and Trep 333 17.6
Rodrigues et al. (2009)23 Brazil Rio de Janeiro 1996 Snowball (HC and MV) Non-trep and Trep 403 7.1
Sanchez et al. (2009)24 Peru Lima 2000 Snowball (HC) Non-trep Q 1056 7.8
Silveira (2002)25 Brazil Sao Paulo 1996 Unknown Non-trep and Trep 1047 9.5
Smith et al. (2010)26 Peru Lima, Callao, Ica 2008 Convenience (MV) Non-trep and Trep 3791 10.0
Snowden et al. (2010)27 Peru Lima, Chiclayo, Trujillo 2005 Targeted (MV) Non-trep and Trep 513 10.5
Solano Chinchilla (2010)28 Costa Rica San José 2009 RDS Non-trep and Trep 300 13.7 (9.7–20.4)
Soto et al. (2007)29 El Salvador San Salvador, Acajutla 2002 Convenience (MV) Non-trep and Trep 347 11.0
Panama Panama, Colón 2002 Convenience (MV) Non-trep and Trep 235 4.9
Guatemala Guatemala, Puerto Barrios, San José 2002 Convenience (MV) Non-trep and Trep 157 13.3
Honduras Tegucigalpa 2002 Convenience (MV) Non-trep and Trep 110 2.7 (0.6–7.8)
Honduras San Pedro 2002 Convenience (MV) Non-trep and Trep 175 5.7 (2.8–10.3)
30
Tabet et al. (2002) Peru Lima 1996 Snowball (MV) Non-trep and Trep 261 8.8
Transgender
COPRESIDA (2009)11 Dominican Santo Domingo, Santiago, La 2008 RDS Non-trep Q 109 9.0 (3.9–16.2)
Republic Altagracia, Barahona
Grandi et al. (2001)31 Brazil Sao Paulo 1998 Snowball (MV) Non-trep and Trep 434 43.3
Ministry of Health, El Salvador (2009)18 El Salvador El Salvador and San Miguel 2008 RDS Non-trep and Trep 92 6.5
Ministry of Health, Nicaragua (2010)19 Nicaragua Managua, Chinandega 2009 Convenience Unknown (active) 78 10.2
Toibaro et al. (2009)32 Argentina Buenos Aires 2006 SS (STI clinic) Non-trep 105 42.3 (28.9–55.7)
Male sex workers
Galban and Benzaken (2007)33 Guatemala Guatemala City 2007 Unknown Unknown - 7.0
Peru 10 cities 2007 Unknown Unknown - 15.9
Ministry of Health, Paraguay (2007)34 Paraguay Concepción, Caaguazú, Itapúa, 2005 Unknown (MV) Unknown 195 13.3
Alto Paraná,
Amambay, Central, Asunción
Female sex workers
Baltazar Reyes et al. (2005)35 Mexico Morelos 1998 Convenience (MV) Non-trep and Trep 100 10.0
Bautista et al. (2009)36 Argentina Buenos Aires, Córdoba, Salta, Rosario, 2002 Snowball (MV) Trep 625 45.7
Mendoza, La Plata
Benzaken et al. (2002)37 Brazil Manacapuru 2000 Cluster (MV) Non-trep 147 0.7
Camejo et al.(2003)38 Venezuela Los Teques 1999 SS (STI clinic) Non-trep and Trep 212 2.4
Campos et al. (2006)39 Peru Huánuco 2005 Targeted (MV) Non-trep and Trep 335 2.2
Pucallpa 2005 Targeted (MV) Non-trep and Trep 387 2.2
Cajamarca, Cerro de Pasco, Chincha, 2005 Targeted (MV) Non-trep and Trep 2960 0.3
Cusco, Ica, Juliaca, Pucallpa, Tumbes
COPRESIDA (2009)11 Dominican Santo Domingo 2008 RDS Non-trep Q 405 5.2
Republic
Santiago 2008 RDS Non-trep Q 301 10.1
Barahona 2008 RDS Non-trep Q 243 5.1
La Altagracia 2008 RDS Non-trep Q 302 11.1
Dutra-Jr et al. (2006)40 Brazil Manaus 2005 RDS Non-trep and Trep 154 18.8
Jiménez Dı́az et al. (2001)41 Mexico Coatzacoalcos 2001 RDS Unknown 196 2.0

A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92


Lahuerta et al. (2011)13 Guatemala Escuintla 2009 SS (STI clinic) Non-trep and Trep 161 1.3
Convenience Non-trep and Trep 438 4.6
(mobile van)
Mejia et al. (2009)42 Colombia Bogotá 2002 Convenience (MV) Non-trep and Trep 514 10.3 (7.8–13.3)
Ministry of Health, Honduras (2008)17 Honduras Comayagua 2006 RDS Non-trep and Trep 212 1.3 (0.0–3.0)
La Ceiba 2006 RDS Non-trep and Trep 181 1.5 (0.4–3.9)
San Pedro 2006 RDS Non-trep and Trep 210 9.8 (3.3–16.5)
Tegucigalpa 2006 RDS Non-trep and Trep 204 11.2 (1.8–15.9)
Ministry of Health, Dominican Dominican Santo Domingo, Distrito Nacional, 2004 SS (STI clinic) Non-trep Q 1110 3.3
Republic (2005)43 Republic La Romana, Puerto Plata, Duarte
Ministry of Health, Dominican Dominican Santo Domingo, Distrito Nacional, 2005 SS (STI clinic) Non-trep Q 1527 2.5
Republic (2006)44 Republic La Romana, Puerto Plata, Duarte
Ministry of Health, Dominican Dominican Santo Domingo, Distrito Nacional, 2006 SS (STI clinic) Non-trep Q 1291 2.0
Republic (2007)45 Republic La Romana, Puerto Plata, Duarte
Ministry of Health, Paraguay (2007)34 Paraguay Concepción, Caaguazú, Itapúa, 2005 Unknown (MV) Unknown 458 19.4
Alto Paraná, Amambay, Central, Asunción
Ministry of Health, Guyana (2004)46 Guyana Demerara 2003 TLS (MV) Non-trep Q 450 15.0
Ministry of Health, El Salvador (2009)18 El Salvador San Salvador 2008 RDS Non-trep and Trep 594 2.7 (1.3–4.4)
Sonsonate 2008 RDS Non-trep and Trep 171 0.7 (0.0–2.2)
Ministry of Health, Nicaragua (2010)19 Nicaragua Chinandega 2009 RDS Non-trep and Trep 213 0.5
Managua 2009 RDS Non-trep and Trep 615 7.0
20
PAHO (unpublished) Colombia Medellin, Barranquilla, Cali, 2008 Cluster (MV) Unknown 1674 18.0
Bucaramanga
Guatemala Guatemala Unknown Unknown Unknown 2663 6.0
Argentina Unknown Unknown Unknown Unknown 1254 26.0
Chile Unknown Unknown Unknown Unknown 9672 0.0
Jamaica Unknown Unknown Unknown Unknown 243 6.0
Sabidó et al. (2009)47 Guatemala Escuintla 2008 SS (STI clinic) Non-trep and Trep 1554 1.1 (0.7–1.6)
Sánchez et al. (2003)48 Peru Lima 1995 SS (STI clinic) Non-trep and Trep 868 4.1
Silva et al. (2007)49 Brazil Santos 1997 Unknown Unknown (active) 1047 12.7
Silveira et al. (2009)50 Brazil Pelotas 2006 Convenience (MV) Trep 322c 7.5
Soto et al. (2007)29 El Salvador San Salvador, Acajutla 2002 TLS (MV) Non-trep and Trep 490 15.0
Guatemala Guatemala, Puerto Barrios, San José 2002 TLS (MV) Non-trep and Trep 522 11.8
Honduras Tegucigalpa, San Pedro, San 2002 TLS (MV) Non-trep and Trep 520 6.0
Lorenzo, Puerto Cortés
Nicaragua Managua, Bluefields, Corinto 2002 TLS (MV) Non-trep and Trep 460 8.4
Panama Panama, Colon 2002 TLS (MV) Non-trep and Trep 431 5.1
Strathdee et al. (2008)51 Mexico Tijuana, Ciudad de Juarez 2004 Convenience (HC) Non-trep and Trep 924 14.0
Tinajeros et al. (2010)52 Honduras Tegucigalpa, San Pedro, La Ceiba 2006 SS (STI clinic) Unknown 378 3.3
2007 SS (STI clinic) Unknown 711 3.7
2008 SS (STI clinic) Unknown 598 0.4
2009 SS (STI clinic) Unknown 429 0.6
2010 SS (STI clinic) Unknown 636 1.4

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e88 A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92

CI, confidence interval; HC, health center; MV, meeting venues; Non-trep, non-treponemal test; Non-trep Q, quantitative non-treponemal test; RDS, respondent-driven sampling; SS, sentinel surveillance (sampling is systematic

One additional study among male sex workers from Sao Paulo, Brazil (reference Grandi et al.31) was not included because it did not meet the sample size (96 participants); syphilis prevalence was 27% using a non-treponemal
Important heterogeneity in testing algorithms was revealed.
Three quarters of the studies reported testing for active syphilis.
% Prevalence

Of the remaining studies, the majority did not specify the kind of
(95% CI)

13.4 test used (19%), or exclusively used a treponemal test (4.2%) or


9.4

2.3
non-treponemal test (3.1%). Twenty-seven studies reported using
signs and symptoms in addition to serology for diagnosis.10,11,13–
19,24,25,28,29,32,35,37,38,40,41,43–49,51
Other studies probably did so as
well, but this was not detailed in the methodology. The sampling
Sample

461

378
400

method also varied, with half of the studies using probability


size

sampling: 31.5% used respondent-driven sampling (RDS), 7.5%


used time–location sampling (TLS), and 3% used cluster sampling.
The other half of the studies used non-probability sampling,
Non-trep and Trep

mostly reporting convenience sampling (18%), sentinel surveil-


Test algorithm

lance (14.5%), snowball sampling (6.5%), and targeted sampling


(5.5%). Thirteen studies did not report any sampling methodology
Non-trep

(13.5%). Among the non-probability sampling studies, partici-


Trep

pants were recruited from meeting venues in 50% of cases,


sexually transmitted infection (STI) clinics and health centers in
43% of cases, and mobile vans in 4.5%; the recruitment venue was
unknown for 2.5%.
Given the heterogeneity of the testing and sampling methods
Convenience (MV)
Convenience (MV)
Type of sampling

used, no statistical tests were applied to test for trends, and only
Targeted (MV)

visual analysis was applied where possible.


(setting)

3.1. Syphilis among men who have sex with men and transgender
populations

Thirty-five records were included for MSM, enrolling a total of


18 527 MSM participants over the period 1998–2010. Rates of
Enrollment

syphilis prevalence were high throughout the period, with no


1998

2007
2008

among health center attendees); STI, sexually transmitted infection; TLS, time–location sampling; Trep, treponemal test.

observed trend (Figure 2). Three quarters of the studies showed


date

active syphilis prevalence of over 4%, and half of them of over 7.5%.
The highest prevalence was found in Peru (Lima, Chiclayo, and
Trujillo), followed by Argentina (Buenos Aires), Costa Rica (San
José), and Guatemala (Puerto Barrios, San José, and Guatemala
Separate study results were not presented for the female and male sex workers included in this study.

City). Cities with the lowest values (<1%) were San Miguel
(El Salvador), Escuintla (Guatemala), and La Ceiba (Honduras).
The three studies among MSM in Lima (Peru) from 1996 to 2007
showed that syphilis prevalence remained high (over 7.8%).
In 11 studies participants were recruited from meeting venues
St-Marc and Gonaives

where MSM congregated, while in another 14 studies a broader


selection of MSM subgroups may have been recruited, given that
Sub-area/city

sampling was through RDS methods.


Soconusco

In 10 studies a range of 1.6% to 33.6% of MSM were reported to


Tijuana

have received money or gifts in exchange for sex,9,10,12,14,16–19,27,29


but only one reported syphilis results separately, with the same
results in both groups.27
This value was not adjusted for the size of the social network.

Five studies were conducted among TG populations, and the


syphilis prevalence was 6.5% in El Salvador, 9.0% in the Dominican
Country

Mexico

Mexico

Republic, 10.2% in Nicaragua, 42.3% in Argentina, and 43.3% in


Haiti

Brazil, representing the highest active syphilis prevalence in the


region among all the study groups. Most of the studies reported a
high percentage of sex work within their sample, but did not
provide separate syphilis prevalence values by sex work.
and treponemal algorithm for testing.

3.2. Syphilis among sex workers and clients of sex workers

Forty-nine studies relating to female sex workers (FSW) were


Uribe-Salas et al. (2003)53
Author (publication date)

Patterson et al. (2009)55

identified, enrolling 40 251 participants over the period 1995–


Couture et al. (2008)54
Clients of sex workers

2010. Half of the studies showed high active syphilis prevalence of


Table 1 (Continued )

over 5%. However, there was a large variation in syphilis


prevalence, both among and within countries. Countries such as
Argentina, Colombia, Paraguay, and Guyana presented very high
syphilis prevalence (over 10%); studies in Jamaica and Panama had
syphilis prevalence between 5% and 10%, and in Peru and Chile,
b
a

studies showed syphilis prevalence of less than 5% and 0%,


A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92 e89

Table 2
Study population — totals

Records, N = 95 Sample size Type of sampling Type of syphilis

MSM, n = 35 MSM, n = 18 527 Convenience: 18% Active: 73.7%


Transgender, n = 5 Transgender, n = 818 Sentinel surveillance: 14.5% Unspecified: 26.3%
MSW, n = 3 MSW, n = 195 Targeted: 6.5% Non-trep test: 3.1%
FSW, n = 49 FSW, n = 40 251 Snowball: 5.5% Trep test: 4.2%
Male and female SW, n = 1 Male and female SW, n = 322 RDS: 31.5% Unknown: 19%
CSW, n = 2 CSW, n = 778 TLS: 7.5%
Cluster: 3%
Unknown: 13.5%

CSW, clients of sex workers; FSW, female sex worker; MSM, men who have sex with men; MSW, male sex worker; Non-trep test, non-treponemal test; RDS, respondent-
driven sampling; SW, sex worker; TLS, time–location sampling; Trep test, treponemal test.

respectively. In most countries there were also considerable and 11.2% in Tegucigalpa in 2006. In 2008, in the Dominican
differences in the prevalence of active syphilis among cities. Brazil Republic the syphilis prevalence was 5% in Barahona and twofold
had one study with a syphilis prevalence of 0.7% in Manacapuru higher in La Altagracia; and in El Salvador prevalence was 0.7% in
(2000) and another study with a prevalence of 18.8% in Manaus Sonsonate and 2.7% in El Salvador.
(2005), two northern cities. Most studies from Mexico showed a Visual analysis could not identify trends among the studies
very high syphilis prevalence – 9.4% in Soconusco and 10.0% in throughout the period 1995–2010 (Figure 3). Only two countries
Morelos (1998) and 14% in Tijuana and Ciudad Juarez (2004); had conducted sentinel surveillance among FSW in consecutive
however a study from Coatzacoalcos showed 2% in 2002. Studies in years, the Dominican Republic (2004–2006) and Honduras (2006–
Guatemala showed 1% syphilis prevalence in Escuintla (2001) and 2010), and both showed statistically significant declines in active
11.8% in Guatemala City, Puerto Barrios, and San José (2002). syphilis and syphilis among FSW, respectively, without specifying
Studies from Honduras showed a prevalence of 1.3% in Comayagua the kind of test used.

Figure 2. Syphilis prevalence among men who have sex with men. TLS: Time location sampling. RDS: Respondent-driven sampling. SS: Sentinel surveillance. SB: Snowball
sampling C: Convenience sampling. T: Targeted sampling.
e90 A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92

Figure 3. Syphilis prevalence among female sexual workers. TLS: Time location sampling. RDS: Respondent-driven sampling. SS: Sentinel surveillance. SB: Snowball sampling
C: Convenience sampling. T: Targeted sampling.

Only three studies provided data on male sex workers (MSW), Sula, Managua, San Salvador, and Acajutla, with high syphilis
reported from Guatemala, Peru, and Paraguay. Their results prevalence in more than one of the MARPs.
showed consistently high rates of syphilis infection, over 7%. Data suggest consistently high syphilis prevalence among MSM
Data are scarce for clients of sex workers; only two studies were throughout the period, particularly in Peru, Argentina, Costa Rica,
found, showing 2.3% and 13.4% of unspecified syphilis prevalence El Salvador, Honduras, Nicaragua, and Guatemala. Similar high
in Tijuana (Mexico) and St-Marc and Gonaives (Haiti), respectively. rates were also reported in other regions worldwide.3,56 Cáceres
Brazil, Argentina, Paraguay, Peru, El Salvador, Guatemala, et al.9 described a disproportionately high prevalence of active
Honduras, and Nicaragua showed cities with a syphilis prevalence syphilis among MSM in Peru. This value could be explained by the
of over 10% in two or more of the four population groups studied. study location. The study took place in low-income neighborhoods
and the participants reported two, three, or four or more sex
4. Discussion partners and a quarter of them had exchanged money for sex in the
past 3 months.
This is the first time that a systematic review has summarized TG persons had the highest syphilis rates of all groups,
data on syphilis prevalence seeking to identify geographical reflecting the augmented vulnerability associated with low self-
distribution in four highly vulnerable populations in LAC. esteem, extreme marginalization, and a lack of legal recognition
The review identified a substantial number of studies in MSM and labor opportunities, which often lead to engagement in
and FSW. Studies were primarily from Latin America. Gaps in the commercial sex work.6 Four of the five studies conducted on the TG
availability of information were identified for Ecuador, Uruguay, population included in this review reported high (over 33.3%)
and Bolivia, as well as for most countries of the Caribbean. participation in sex work.9,13,28,29
When analyzing chronological trends, data showed that syphilis Most of the literature in LAC focuses on FSW and not on MSW
infection is well-established in LAC, specifically in MARPs. Despite (49 vs. 3 studies). Among FSW, data support a wide variation in
efforts towards HIV/STI control,3 successful control of syphilis active syphilis prevalence among and within countries, ranging
infection does not appear to be reflected in this work. The review from 0.3% to 18.8%. Far less attention is paid to the health issues of
identified critical cities as ‘hotspots’, such as Sao Paulo, Buenos Aires, MSW, who often face double discrimination because of sexual
Guatemala City, Puerto Barrios, San José (Guatemala), San Pedro orientation and type of work.3,57,58
A.C. Zoni et al. / International Journal of Infectious Diseases 17 (2013) e84–e92 e91

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