Literature DB >> 25471736

Risk factors associated with prevalent and incident syphilis among an HIV-infected cohort in Northeast China.

Qing-hai Hu1,2, Jun-jie Xu3,4, Hua-chun Zou5, Jing Liu6,7, Jing Zhang8,9, Hai-bo Ding10,11, Han-Zhu Qian12, Si-ruo Li13, Yu Liu14, Yong-jun Jiang15,16, Hong Shang17,18, Ning Wang19,20.   

Abstract

BACKGROUND: Sexually transmitted infections (STIs) increase HIV infectivity through local inflammatory processes. Prevalent and incident STIs among people who live with HIV/AIDS (PLWHA) are indicators of high-risk sexual behaviors and imply potential spread of HIV. Little is known about the prevalence and incidence of concurrent syphilis and associated risk behaviors among PLWHA in China.
METHODS: A retrospective cohort study was conducted among PLWHA who attended the outpatient clinic of a designated AIDS treatment hospital in Shenyang, China, between March 2009 and May 2013. Physical examinations and syphilis serology were conducted at each visit. A questionnaire on demographic characteristics was also collected.
RESULTS: A total of 1010 PLWHA were enrolled, of whom 77.0% were men who have sex with men (MSM). The baseline syphilis prevalence among PLWHA was 19.8% (95% confidence interval [CI]:17.3-22.3%). During follow-up, 78.3% retained in the cohort, and contributed a median follow-up of 9.4 months (interquartile range: 5.9-18.7 months). Syphilis incidence among PLWHA was 18.7 (95% CI: 15.5-21.8) per 100 person years. Mulitvariate logistic analysis showed that receiving antiretroviral therapy (ART) (adjusted OR [aOR] = 0.48), older age (≥40 years vs. ≤24 years, aOR = 2.43), being MSM (aOR = 2.30) and having higher baseline HIV viral load (>100,000 copies/mL vs. ≤100,000 copies/mL, aOR = 1.56) were independent predictors for syphilis infection among PLWHA at enrollment (p < 0.05 for all). Mulivariate Cox regression found that receiving ART (adjusted hazard ratio [aHR] = 1.81), older age (≥40 years vs. ≤24 years, aHR: 5.17) and MSM status (aHR = 2.68) were independent risk factors for syphilis seroconversion (each p < 0.05).
CONCLUSIONS: Syphilis prevalence and incidence were high among PLWHA in Shenyang. A campaign focusing on detection and treatment of syphilis among PLWHA is urgently needed, especially one with a focus on MSM who are at a higher risk for syphilis.

Entities:  

Mesh:

Year:  2014        PMID: 25471736      PMCID: PMC4265485          DOI: 10.1186/s12879-014-0658-1

Source DB:  PubMed          Journal:  BMC Infect Dis        ISSN: 1471-2334            Impact factor:   3.090


Background

China has witnessed a rapid increase of sexually transmitted infections (STIs), including syphilis and HIV in the past decade [1],[2]. The national sentinel surveillance in 2009 showed that syphilis prevalence was 2.4% among female sex workers (FSWs), 3.4% among people who inject drugs (PWID), and 9.1% among men who have sex with men (MSM) [1]. The population prevalence of syphilis in China was 32.0 per 100,000 people in 2011 [3] which was over 7 times as high as that in the US (4.5 per 100,000 people) [4] and the UK (5.6 per 100,000 people) [5]. In 2008, the prevalence of active syphilis among MSM was 12.2% in China, which was lower than that in Thailand (21.6%) but higher than that in Indonesia (4.0%) [6]. Sexual transmission had become the major route of HIV transmission in China in recent years [7]. Of 70,000 newly reported HIV/AIDS cases in the first nine months of 2013, heterosexual transmission accounted for 69.1% and MSM transmission accounted for 20.8% of all cases [8]. Globally the majority of HIV prevention programs usually focus on HIV negative individuals who are at high risk for HIV infection [9],[10]. However, recently researchers realized that it may be more efficient to prevent HIV if we target people living with HIV/AIDS (PLWHA) (“positive prevention”), as they really serve as the sources of HIV transmission [11]. A meta-analysis showed that positive preventions were efficacious in reducing unprotected sex and acquisition of STIs [12]. The concept of Treatment as prevention strategy was raised and investigated quite intensively in recent years, and antiretroviral therapy (ART) can remarkably decrease the risk of transmitting HIV through reducing viral load (VL) among PLWHA [13],[14]. HIV-1 RNA in seminal plasma may decline more slowly than that in blood and could be detected with undetectable HIV-1 RNA in blood plasma when PLWHA experience ART [15],[16], which points to the potential risk for HIV transmission via unprotected sexual behaviors. Moreover, ART may lead to complacent as people feel that they may live a long life with HIV and restore sexual desire as well as physical and immunological functions [17],[18]. Because of sharing a common mode of sexual transmission, syphilis and HIV infection have significant epidemic synergistic. Syphilis incidence is considered an indicator of high-risk sexual behaviors [19],[20]. Therefore, it is useful to understand the risk for HIV transmission among PLWHA by measuring their risk for syphilis transmission [21]. In addition, among individuals diagnosed with HIV who are not yet eligible for ART, treatment of co-infections including syphilis may offer an important alternative approach to reducing HIV VL and decreasing HIV transmission risk [22]. Little is known about the risk for syphilis transmission among PLWHA and its correlation with ART and sexual behaviors [23]. In this retrospective cohort study we aimed to evaluate both syphilis prevalence and incidence among PLWHA in Northeast China.

Methods

Study population and participants enrollment

This retrospective cohort study was conducted among HIV-infected patients in Shenyang City in Northeast China. HIV status was based on positive test results from two peripheral blood samples by HIV ELISA and confirmed by western blot (Gene labs Diag. Singapore). All HIV testing sites were certified by the National AIDS Reference Laboratory at China CDC. Participants were recruited from The First Affiliated Hospital of China Medical University (CMU), which was one of two designated hospitals providing free ART in Shenyang City. Since 2002, PLWHA in China with a CD4+ T cell counts of 200 cells/mm3 or less, total lymphocyte counts of less than 1200 cells/mm3, or WHO disease stage 3 or 4 have been eligible for free combination antiretroviral therapy. In 2008, the CD4+ T cell counts threshold for treatment was increased to 350 cells/mm3 [24]. Between March 2009 and May 2013, patients who were scheduled for a regular visit at the HIV outpatient clinic in The First Affiliated Hospital of CMU were invited to participate in a baseline assessment. Eligible participants were those who: were 18 years or older and were able and willing to provide written informed consent. Baseline syphilis serological test was conducted to assess prevalent syphilis. Syphilis un-infected patients were followed up every 6 months to assess incident syphilis. During the follow-up, we calculated survival as time from baseline initiation to syphilis seroconversion or censoring. Patients were censored at dropout, loss to follow-up, or on May 31, 2013, whichever came first. Those who were diagnosed with syphilis infection were referred to the STI clinic in the same hospital for treatment. Figure 1 shows the study procedures.
Figure 1

Procedure of enrollment and follow-up. A total of 1302 participants were invited, 243 did not meet enrollment criteria, 49 declined enrollment. A total of 1010 participants were included at baseline. Of the 810 participants who were syphilis seronegative at baseline, 634 completed at least one follow-up visit.

Procedure of enrollment and follow-up. A total of 1302 participants were invited, 243 did not meet enrollment criteria, 49 declined enrollment. A total of 1010 participants were included at baseline. Of the 810 participants who were syphilis seronegative at baseline, 634 completed at least one follow-up visit. Ethical approval was obtained from the institutional review board of The First Affiliated Hospital of CMU prior to the commencement of the study.

Data collection

At baseline, patients were asked to self-complete an anonymous questionnaire on demographic characteristics, HIV history including date and venues of HIV diagnosis, transmission route, and ART experience. HIV VL and CD4+ T cell counts were also tested as part of regular care. The blood specimens collected at baseline and 6-monthly follow-up visits were also tested for syphilis infection. After explanation of study, informed consent was obtained from all participants.

Laboratory testing

Syphilis screening serological test was performed using rapid plasma reagin (RPR; Shanghai Kehua Bio-engineering Co., Ltd, China). Positive RPR results were confirmed using Treponema Pallidum particle assay (Serodia TPPA; Fujirebio, Tokyo, Japan). Subjects who were plasma positive for both TPPA and RPR were considered as current infection. RPR negative participants at baseline who turned to be positive for both TPPA and RPR at follow-up visits were defined as syphilis seroconversion event. In addition, TPPA negative participants at baseline who turned to be TPPA positive were eligible for syphilis seroconversion during the follow-up period. CD4+ T cell counts were determined by flow cytometry (BD Bioscience San Diego, CA, USA). Plasma HIV-1 RNA copy was measured by a commercial HIV RNA quantitative detection assay, COBAS AmpliPrep/COBAS TaqMan HIV-1 Test (Roche, Germany), with a detection limit of 40 copies/mL in plasma. All tests were performed according to the manufacturers’ instructions.

Data analysis

Demographic and HIV history variables were compared between participants with prevalent syphilis at baseline and those without; and between those who seroconverted during follow-up and those who did not. We analyzed covariates including sex, age (≤24, 25–39, and ≥40 years), ethnicity, marital status, occupation, education, HIV transmission route (heterosexual, MSM and others), HIV diagnosis venues (voluntary counseling and testing [VCT], hospital, others and unknown), baseline CD4+ T cell counts (<200, 200-349, 350–499, and ≥500 counts/mm3), baseline VL (≤100000 and >100000 copies/mL). Logistic regression was performed to assess factors associated with prevalent syphilis infection at baseline. Cox proportional hazard regression was used to determine the adjusted hazard ratio (aHR) for factors associated with incident syphilis infection. Syphilis seroconversion was estimated to occur at the midpoint of the interval between the last negative test and the subsequent follow-up positive test. Syphilis incidence rate and its 95% confidence interval (CI) were calculated assuming Poisson distribution. Variables with P < 0.20 in univariate analysis were included in the multivariate logistic or Cox regression models. Only variables with P < 0.05 were kept in the final multivariate models. Double data entries were performed using EpiData software (The Epi Data Association Odense, Denmark, version 3.02). Data were analyzed using SAS 9.1 (SAS Institute Inc., Cary, NC).

Results

Demographic characteristics of study participants

As shown in Figure 1, a total of 1302 PLWHA who were registered at the HIV clinic were invited to participate in the study, 243 did not meet enrollment criteria, 49 declined enrollment. Therefore a total of 1010 participants were included in the estimation of HIV prevalence at baseline. Of the 810 participants who were syphilis seronegative at baseline, 78.3% (634/810) completed at least one follow-up visit and contributed a median follow-up of 9.4 months (interquartile range [IQR]: 5.9-18.7 months). Table 1 shows the demographic characteristics and HIV history stratified by syphilis serostatus at baseline and syphilis seroconversion during follow-up. At baseline, the median age was 35 years (IQR: 27-46); 87.4% were ethnic Han; 93.3% were male; 87.6% were Shenyang residents, 34.8% had an education of high school or higher; 51.7% were single, 32.7% were currently married and 15.6% were divorced; 77.0% self-reported as being MSM.
Table 1

Characteristics of PLWHA with prevalent and incident syphilis in Shenyang

CharacteristicSyphilis infection at baselineSyphilis seroconversion during follow-up
No. of participantsSeropositive casesPrevalence (%)No. of participantsPerson–years (PY)Incident casesIncidence (per 100 PY)
Overall 101020019.8634702.313118.7
Gender
 Female6845.95140.637.4
 Male94219620.8583661.812819.3
Age (year)
Median(IQR)35(27-46)35(27-46)
 ≤241422215.592124.886.4
 25-394617716.7299353.74312.2
 ≥4040710124.8243223.98035.7
Ethnicity
 Han88318220.6552607.011519.0
 Other ethnicities1271814.28295.31616.8
Marital status
 Single52210219.5317376.05414.4
 Married3306218.8213219.34420.1
 Divorced1583622.8104107.13330.8
Occupation
 Employed64512920.0415461.39019.5
 Unemployed1983618.2123120.02420.0
 Retired762229.04346.51430.1
 Student911314.35374.734.0
Education
 Less than high school3517721.9209225.44620.4
 High school or more65912318.7425476.98517.8
Shenyang resident
 Yes88518120.5560601.411519.1
 No1251915.274100.91615.9
HIV transmission route
 Heterosexual1461611.010388.21517.0
 MSM77817122.0478570.011119.5
 Others (injection drug use, blood, unknown)861315.15344.2511.3
HIV diagnosis venue
 VCT2775419.5182244.94116.7
 Hospital3668723.8242281.35921.0
 Others (blood donation, physical exam, etc.)57610.54870.057.2
 Unknown3105317.1162106.22624.5
ART at baseline
 No68715923.1385501.06813.6
 Yes3234112.7249201.36331.3
Time since HIV diagnosis (year)
 ≤273015621.4439514.17915.4
 >22804415.7195188.25227.6
Baseline CD 4 + T cell counts(counts/mm 3 )
 ≥5001522818.495126.32021.1
 350-4992554015.7173194.14123.7
 200-3493316218.7214226.73616.8
 <2002466526.4142137.73021.1
 Unknown26519.21017.5440.0
Baseline VL (copies/mL)
 ≤100,00059911819.7378455.67716.9
 >100,0001484631.17285.51315.2
 Unknown2633613.7184161.24125.4

IQR: interquartile range; VCT: voluntary counseling and testing; ART: antiretroviral therapy; VL: viral load; PY: person year.

Characteristics of PLWHA with prevalent and incident syphilis in Shenyang IQR: interquartile range; VCT: voluntary counseling and testing; ART: antiretroviral therapy; VL: viral load; PY: person year. Just over a quarter (27.4%) of participants had been diagnosed with HIV at VCT venues, 36.2% in hospitals, and the rest through other ways such as HIV/AIDS research projects. Nearly one third (32.0%) had prior ART. At baseline 15.1%, 25.3%, 32.8% and 24.4% had a CD4+ T cell counts of ≥500, 350-499, 200-349 and <200 cells/mm3, respectively. CD4+ T cells were not detected in 2.6% of participants. At baseline 59.3% and 14.7% had a VL of ≤100,000 and >100,000 copies/mL, respectively. VL was not detected in 26.0% of participants.

Factors associated with seropositivity of syphilis at baseline

The baseline seroprevalence of syphilis was 19.8% (95% CI: 17.3–22.3%). Table 2 illustrates the factors associated with baseline syphilis infection. In the final multivariate logistic regression model, ART experience was negatively associated with syphilis infection (adjusted OR [aOR] = 0.48, 95% CI: 0.31–0.73), but older age (≥40 years vs. ≤24 years) (aOR = 2.43, 95% CI: 1.42–4.15), being MSM (aOR = 2.30, 95% CI: 1.30–4.08), and having higher baseline VL (>100,000 copies/mL vs. ≤100000 copies/mL) (aOR = 1.56, 95% CI: 1.02–2.40) were independently associated with a higher risk of syphilis infection (each p < 0.05).
Table 2

Factors associated with syphilis infection at baseline among PLWHA in Shenyang

FactorOR (95% CI) P -valueAdjusted OR (95% CI) P -value
Gender
 Female1.00
 Male4.20 (1.51 –11.69)0.006
Age(year)
 ≤24 years1.00
 25-39 years1.09 (0.65 -1.83)0.7341.26 (0.74 –2.12)0.395
 ≥40 years1.80 (1.08 -2.99)0.0232.43 (1.42 –4.15)0.001
Ethnicity
 Han1.00
 Other ethnicities0.64 (0.38 –1.08)0.091
Marital status
 Single1.00
 Married0.95 (0.67 –1.35)0.786
 Divorced1.22 (0.79 –1.87)0.375
Occupation
 Employed1.00
 Unemployed0.89 (0.59 –1.34)0.573
 Retired1.63 (0.96 –2.77)0.072
 Student0.67 (0.36 –1.24)0.199
Education
 Less than high school1.00
 High school or more0.82 (0.59 –1.12)0.214
Shenyang resident
 Yes1.00
 No0.70 (0.42 –1.17)0.170
HIV transmission route
 Heterosexual1.00
 MSM2.29 (1.33 –3.95)0.0032.30 (1.30 –4.08)0.004
 Others (injection drug use, blood, unknown)1.45 (0.66 –3.18)0.3571.33 (0.59 –2.97)0.488
HIV Diagnosis venue
 VCT1.00
 Hospital1.29 (0.88 –1.89)0.1951.42 (0.94 –2.13)0.095
 Others (blood donation, physical exam, etc.)0.49 (0.20 –1.19)0.1150.63 (0.25 –1.56)0.314
 Unknown0.85 (0.56 –1.30)0.4530.75 (0.49 –1.17)0.208
ART at baseline
 No1.00
 Yes0.48 (0.33 –0.70)<0.0010.48 (0.31 –0.73)0.001
Time since HIV diagnosis (year)
 ≤21.00
 > 20.69 (0.48 –0.99)0.044
Baseline CD 4 + T counts(counts/ mm 3 )
 ≥5001.00
 350-4990.82 (0.48 –1.40)0.475
 200-3491.02 (0.62 –1.67)0.935
 <2001.59 (0.97 –2.62)0.068
 Unknown1.05 (0.37 –3.04)0.922
Baseline VL(copies/mL)
 ≤1000001.00
 >1000001.84 (1.23 -2.75)0.0031.56 (1.02 –2.40)0.040
 Unknown0.65 (0.43 -0.97)0.0350.82 (0.54 –1.26)0.361

VCT: voluntary counseling and testing; ART: antiretroviral therapy; VL: viral load.

Factors associated with syphilis infection at baseline among PLWHA in Shenyang VCT: voluntary counseling and testing; ART: antiretroviral therapy; VL: viral load.

Factors associated with seroconversion of syphilis during follow-up

Of the 634 eligible participants for syphilis incidence estimation, 131 (20.7%) seroconverted during follow-up. The incidence rate was 18.7 (95% CI: 15.5–21.8) per 100 person years (PY). Table 3 shows factors associated with syphilis seroconversion. ART experience (adjusted hazard ratio [aHR] = 1.81, 95% CI: 1.25–2.62), older age (≥40 years vs. ≤24 years) (aHR = 5.17, 95% CI: 2.47–10.84), and being MSM (aHR: 2.68, 95% CI: 1.53–4.69) were independently associated with syphilis seroconversion (each p < 0.05).
Table 3

Factors associated with syphilis seroconversion among PLWHA in Shenyang

FactorHR (95% CI)P-valueAdjusted HR (95% CI)P-value
Gender
 Female1.00
 Male3.39 (1.08 –10.65)0.037
Age (year)
 ≤24 years1.00
 25-39 years1.79 (0.84 -3.81)0.1311.86 (0.87 –3.98)0.108
 ≥40 years4.85 (2.34 -10.05)<0.0015.17 (2.47 –10.84)<0.001
Ethnicity
 Han1.00
 Other ethnicities0.91 (0.54 –1.53)0.713
Marital status
 Single1.00
 Married1.31 (0.88 –1.95)0.183
 Divorced2.00 (1.29 –3.08)0.002
Occupation
 Employed1.00
 Unemployed0.98 (0.62 –1.54)0.924
 Retired1.58 (0.90 –2.77)0.112
 Student0.23 (0.07 –0.72)0.012
Education
 Less than high school1.00
 High school or more0.89 (0.62 –1.27)0.503
Shenyang resident
 Yes
 No0.89 (0.53 –1.51)0.676
HIV transmission route
 Heterosexual1.00
 MSM1.45 (0.84 –2.49)0.1812.68 (1.53 –4.69)0.001
 Others (injection drug use, blood, unknown)0.68 (0.25 –1.87)0.4550.63 (0.23 –1.75)0.376
HIV Diagnosis venue
 VCT1.00
 Hospital2.82 (1.13 -7.03)0.0262.08 (0.83 –5.22)0.120
 Others (blood donation, physical exam, etc.)2.34 (0.92 -5.91)0.0731.92 (0.76 –4.87)0.171
 Unknown3.05 (1.17 -7.98)0.0232.55 (0.97 –6.74)0.058
ART at baseline
 No1.00
 Yes1.81 (1.27 –2.57)0.0011.81 (1.25 –2.62)0.002
Time since HIV diagnosis (year)
 ≤21.00
 > 21.57 (1.10 –2.23)0.012
Baseline CD 4 + T cell counts(counts/mm 3 )
 ≥5001.00
 350-4991.26 (0.74 –2.16)0.392
 200-3490.92 (0.53 –1.59)0.764
 <2001.26 (0.71 –2.22)0.428
 Unknown1.83 (0.62 –5.36)0.272
Baseline VL(copies/mL)
 ≤1000001.00
 >1000000.97 (0.54 –1.75)0.920
 Unknown1.28 (0.87 –1.87)0.207

VCT: voluntary counseling and testing; ART: antiretroviral therapy; VL: viral load.

Factors associated with syphilis seroconversion among PLWHA in Shenyang VCT: voluntary counseling and testing; ART: antiretroviral therapy; VL: viral load.

Discussion

STIs pose considerable health threats to PLWHA. In this study, we report on the first evaluation of both syphilis prevalence and incidence among an HIV-infected cohort in northeast China. The prevalence among PLWHA in Shenyang (19.8%) is much higher than that among PLWHA in Taiwan (5.7%) [25], Guangzhou (10.5%) [26] and Liuzhou City (11.4%) [27] in China. It is also higher than the average syphilis prevalence among PLWHA from a Meta analysis (9.5%) [28]. Syphilis incidence among Shenyang PLWHA (18.7/100 PY) is significantly higher than that in Seoul, South Korea (4.57/100 PY) [29], and higher than the syphilis incidence among Sichuan PWID (4.71/100 PY) [30] and Xichang FSWs (6.23/100 PY) [31]. Syphilis can generate genital ulcers and increase the likelihood of HIV virus shedding. Additionally syphilis co-infection among PLWHA can increase the concentration of HIV RNA in blood plasma and decrease the number of CD4+ T cell counts [22], and may increase the risk for HIV transmission [32]. It’s highly likely that high prevalent and incident syphilis may contribute to the spread of HIV which is a new threat to HIV prevention. Our findings provide important information to the development of syphilis screening and treatment program for PLWHA across China. Syphilis is a marker of unsafe sexual practices [20],[21], and therefore the high syphilis prevalence and incidence indicated that PLWHA who had already known self HIV positive status may still engage in unprotected sex. Behavioral intervention can reduce HIV transmission risk among HIV positive MSM [33]. Efficient education programs including safer sexual behavioral interventions are urgently needed to reduce risk for STIs transmission among PLWHA in China. Conflicting results are provided by studies analyzing the association between ART experience and STIs transmission [34]-[36]. Our data show that the syphilis seropositive rate among ART patients was significantly lower than that among treatment naïve patients. The possible reasons for this may include: unrecovered immune status, degenerative sexual desires and lower frequency of unprotected sexual behaviors. Our study further shows that PLWHA who took ART had significantly increased syphilis incidence. This is consistent with the findings by Stolte, et al. in Amsterdam [34], but inconsistent with that by Huang, et al. in Taiwan [37]. Though ART correlate with substantially lowered HIV RNA levels and decreased HIV infectiveness among PLWHA [13],[14], apart from beneficial clinical effects, treatment advances may have unintended effects on sexual behavior. Some evidence suggests that since ART became available, the prevalence of unprotected sex [34],[38] have increased. Sexually transmitted co-infections increase HIV infectiveness through local inflammatory processes and offset the ART treatment effect as being HIV secondary prevention. These findings suggest that, with the expansion of ART in China, health education, behavioral interventions and STIs monitoring should be strengthened among ART patients. MSM (vs. heterosexual), current use of ART at baseline, and older age (≥40 vs. ≤24 years) were independently correlated with baseline syphilis infection. MSM status is also a risk factor for incident syphilis infection, which is consistent with the literature [36],[39]. In China MSM accounted for 0.3% of the total reported HIV/AIDS cases in 2006. This figure rapidly increased to 13.0% in 2011 [7]. A large number of MSM engage in unprotected sexual behaviors and multiple sexual partnership [40],[41] which place them at risk for both HIV and syphilis infections. Our findings suggest that HIV-infected MSM should be given priority to receive syphilis screening and treatment in Shenyang city. This study found that the participants aged 40 or older had a significantly higher risk for syphilis than patients aged 24 or younger. HIV infections among the elderly have become increasingly common in China in recent years [7],[42],[43]. The possible reasons for higher risks for HIV and STIs among elderly may include increasing use of commercial sex, infrequent condom use and low uptake of STIs testing [42]-[44]. Our study has limitations. Firstly, we did not collect data on sexual behaviors and therefore couldn’t evaluate the relationship between syphilis and sexual behaviors. Secondly, the participants were a convenience sample of PLWHA who lived in Shenyang city. Results from this study may not represent all individuals who are living with HIV/AIDS in China. Thirdly, higher loss to follow-up is another challenge in our study. By the end of the study period, about 21.7% of the participants were lost to follow-up, and this may cause selection bias. Fourthly, because HIV and syphilis are sensitive topic for participants, this study cannot exclude social desirability bias. Our study, with data on both syphilis prevalence and incidence in HIV-infected population, provides significant evidence for improving HIV/STIs prevention interventions and care, albeit with above-mentioned limitations.

Conclusions

The prevalence and incidence of concurrent syphilis were both moderately high among PLWHA in Northeast China. Results from this program suggest that receiving ART, older age, and MSM status were independent risk factors for both prevalent and incident syphilis infection. Interventions focusing on the detection and treatment of syphilis are urgently needed for PLWHA in China, especially MSM who are at high risk for syphilis.
  36 in total

1.  Impact of highly active antiretroviral treatment on HIV seroincidence among men who have sex with men: San Francisco.

Authors:  Mitchell H Katz; Sandra K Schwarcz; Timothy A Kellogg; Jeffrey D Klausner; James W Dilley; Steven Gibson; William McFarland
Journal:  Am J Public Health       Date:  2002-03       Impact factor: 9.308

2.  HIV prevention for a threatened continent: implementing positive prevention in Africa.

Authors:  Rebecca Bunnell; Jonathan Mermin; Kevin M De Cock
Journal:  JAMA       Date:  2006-08-16       Impact factor: 56.272

Review 3.  Do prevention interventions reduce HIV risk behaviours among people living with HIV? A meta-analytic review of controlled trials.

Authors:  Nicole Crepaz; Cynthia M Lyles; Richard J Wolitski; Warren F Passin; Sima M Rama; Jeffrey H Herbst; David W Purcell; Robert M Malow; Ron Stall
Journal:  AIDS       Date:  2006-01-09       Impact factor: 4.177

4.  [A prospective cohort study on human immunodeficiency virus and syphilis seroconversion among injecting drug users].

Authors:  Lu Yin; Guang-ming Qin; Yu-hua Ruan; Li Zhang; Qin-ning Hao; Xian-huang Chen; Zheng-qing Jiang; Ben-li Song; Shi-zhu Liu; Xiao-yun Cao; Chun Hao; Kang-lin Chen; Yi-ming Shao
Journal:  Zhonghua Liu Xing Bing Xue Za Zhi       Date:  2006-04

5.  Increase in sexually transmitted infections among homosexual men in Amsterdam in relation to HAART.

Authors:  I G Stolte; N H Dukers; J B de Wit; J S Fennema; R A Coutinho
Journal:  Sex Transm Infect       Date:  2001-06       Impact factor: 3.519

6.  Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections.

Authors:  Kate Buchacz; Pragna Patel; Melanie Taylor; Peter R Kerndt; Robert H Byers; Scott D Holmberg; Jeffrey D Klausner
Journal:  AIDS       Date:  2004-10-21       Impact factor: 4.177

7.  Highly active antiretroviral therapy and sexual risk behavior: a meta-analytic review.

Authors:  Nicole Crepaz; Trevor A Hart; Gary Marks
Journal:  JAMA       Date:  2004-07-14       Impact factor: 56.272

8.  High levels of unprotected sex with men and women among men who have sex with men: a potential bridge of HIV transmission in Beijing, China.

Authors:  Kyung-Hee Choi; David R Gibson; Lei Han; Yaqi Guo
Journal:  AIDS Educ Prev       Date:  2004-02

9.  Recent acquired STD and the use of HAART in the Italian Cohort of Naive for Antiretrovirals (I.Co.N.A): analysis of the incidence of newly acquired hepatitis B infection and syphilis.

Authors:  P Cicconi; A Cozzi-lepri; G Orlando; A Matteelli; E Girardi; A Degli Esposti; C Moioli; G Rizzardini; A Chiodera; G Ballardini; C Tincati; A d'Arminio Monforte
Journal:  Infection       Date:  2008-01-29       Impact factor: 3.553

10.  Refocusing health promotion for syphilis prevention: results of a case-control study of men who have sex with men on England's south coast.

Authors:  J Imrie; N Lambert; C H Mercer; A J Copas; A Phillips; G Dean; R Watson; M Fisher
Journal:  Sex Transm Infect       Date:  2006-02       Impact factor: 3.519

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  14 in total

1.  Syphilis and HIV: Is HAART at the heart of this epidemic?

Authors:  Susan Tuddenham; Maunank Shah; Khalil G Ghanem
Journal:  Sex Transm Infect       Date:  2017-01-16       Impact factor: 3.519

2.  High polymorphism rates in well-known T cell epitopes restricted by protective HLA alleles during HIV infection are associated with rapid disease progression in early-infected MSM in China.

Authors:  Chuan He; Xiaoxu Han; Hui Zhang; Fanming Jiang; Minghui An; Bin Zhao; Haibo Ding; Zining Zhang; Tao Dong; Hong Shang
Journal:  Med Microbiol Immunol       Date:  2019-03-08       Impact factor: 3.402

3.  Investigating latent syphilis in HIV treatment-experienced Ethiopians and response to therapy.

Authors:  Selamawit Girma; Wondwossen Amogne
Journal:  PLoS One       Date:  2022-07-12       Impact factor: 3.752

4.  Syphilis on the rise: A prolonged syphilis outbreak among HIV-infected patients in Northern Greece.

Authors:  Olga Tsachouridou; Lemonia Skoura; Eirini Christaki; Panagiotis Kollaras; Eleni Sidiropoulou; Pantelis Zebekakis; Efstratios Vakirlis; Apostolia Margariti; Symeon Metallidis
Journal:  Germs       Date:  2016-09-01

5.  Incidence and Risk Factors for Incident Syphilis among HIV-1-Infected Men Who Have Sex with Men in a Large Urban HIV Clinic in Tokyo, 2008-2015.

Authors:  Takeshi Nishijima; Katsuji Teruya; Satoshi Shibata; Yasuaki Yanagawa; Taiichiro Kobayashi; Daisuke Mizushima; Takahiro Aoki; Ei Kinai; Hirohisa Yazaki; Kunihisa Tsukada; Ikumi Genka; Yoshimi Kikuchi; Shinichi Oka; Hiroyuki Gatanaga
Journal:  PLoS One       Date:  2016-12-16       Impact factor: 3.240

6.  Factors associated with syphilis incidence in the HIV-infected in the era of highly active antiretrovirals.

Authors:  Mohaned Shilaih; Alex Marzel; Dominique L Braun; Alexandra U Scherrer; Helen Kovari; Jim Young; Alexandra Calmy; Katharine Darling; Manuel Battegay; Matthias Hoffmann; Enos Bernasconi; Maria C Thurnheer; Huldrych F Günthard; Roger D Kouyos
Journal:  Medicine (Baltimore)       Date:  2017-01       Impact factor: 1.889

Review 7.  A double-edged sword: does highly active antiretroviral therapy contribute to syphilis incidence by impairing immunity to Treponema pallidum?

Authors:  Michael L Rekart; Wilfred Ndifon; Robert C Brunham; Jonathan Dushoff; Sang Woo Park; Sanjana Rawat; Caroline E Cameron
Journal:  Sex Transm Infect       Date:  2017-01-16       Impact factor: 3.519

8.  Risky sexual networks and concentrated HIV epidemics among men who have sex with men in Wenzhou, China: a respondent-driven sampling study.

Authors:  Qiaoqin Ma; Shidian Zeng; Shichang Xia; Xiaohong Pan; Dayong Wang; Haishen Zhu; Hui Wang; Tingting Jiang; Lin He; Dongshe Zhao; Zhihang Peng
Journal:  BMC Public Health       Date:  2015-12-16       Impact factor: 3.295

9.  The tradition algorithm approach underestimates the prevalence of serodiagnosis of syphilis in HIV-infected individuals.

Authors:  Bin Chen; Xiuming Peng; Tiansheng Xie; Changzhong Jin; Fumin Liu; Nanping Wu
Journal:  PLoS Negl Trop Dis       Date:  2017-07-20

10.  Serum TRSUT Titer ≥1: 16 Is a Predictor for Neurosyphilis Among HIV-Infected Patients With Concurrent Syphilis and No Neurological Symptoms.

Authors:  Jian-Jun Sun; Zhen-Yan Wang; Jia-Yin Shen; Yin-Zhong Shen; Li Liu; Jiang-Rong Wang; Ren-Fang Zhang; Hong-Zhou Lu
Journal:  Medicine (Baltimore)       Date:  2015-11       Impact factor: 1.817

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