JEADV
DOI: 10.1111/jdv.12745
ORIGINAL ARTICLE
Primary syphilis in HIV-negative patients is on the rise in Greece: epidemiological data for the period 2005–2012 from a tertiary referral centre in Athens, Greece A. Kanelleas,* C. Stefanaki, I. Stefanaki, G. Bezrondii, V. Paparizos, A. Arapaki, Z. Kripouri, C. Antoniou, E. Nicolaidou 1st Department of Dermatology and Venereology, Sexually Transmitted Infections Unit, University of Athens School of Medicine, ‘A. Sygros’ Hospital, Athens, Greece *Correspondence: A. Kanelleas. E-mail: [email protected]
Abstract Background Epidemiological data on primary syphilis in Greece are limited. Objective The purpose of the present study was to investigate the trends of the disease in Greece during the last few years and whether they are in accordance with the trends in other European countries and the United States of America. Methods We conducted a retrospective analysis based on records of patients who visited the Sexually Transmitted Infections Unit of ‘A. Sygros’ Hospital in Athens, Greece, during the period 2005–2012. Our hospital is a tertiary referral centre for sexually transmitted infections covering an area of more than four million people, which is almost half the population of Greece. We documented the total annual number of patients, the male to female ratio, sexual orientation, patients’ ethnic origin and education level. Results We reviewed the records of 1185 patients with a confirmed diagnosis of primary syphilis. The total number of patients with primary syphilis has risen from 111 in 2005 to 158 in 2012, an increase of 42.3%. The mean annual number is 148. The mean male to female ratio is 4.76 : 1, with a peak value of 8.50 : 1 in 2011. The majority of patients are of Greek origin, ranging from 67.4% to 87.2%. Within the male patients group, it seems that the percentage of men having sex with men has risen steadily from 2005 (20.7%) up to 2010 (59.1%) with a decline in 2012 (46.0%). The mean value over 8 years is 45.0%. Conclusion Primary syphilis in Greece is on the rise. Τhe majority of our patients are Greek, despite immigrant influx. Men clearly outnumber women, representing more than 80% of the total number of patients. Furthermore, there seems to be a trend towards predominance of men having sex with men as the core group among male patients. Received: 21 April 2014; Accepted: 12 August 2014
Conflicts of interest None declared.
Funding sources None declared.
Introduction Syphilis is a sexually transmitted infection (STI) caused by the spirochaeta Treponema pallidum. In most countries of the European Union (EU) and the European Economic Area (EEA), all new cases of primary syphilis (PS) and congenital syphilis are compulsorily reported to national authorities. Then, the European Centre for Disease Control (ECDC) is notified on an annual basis. Unfortunately, not all EU-EEA countries have comprehensive, active and case-based surveillance systems that provide coverage on a national level. The data from Greece that are included in the 2013 Annual Epidemiological Report are based on a passive
JEADV 2014
and aggregated surveillance system that gathers data mainly from STI-dedicated clinics in Skin and Venereal Diseases Hospitals. There are two such hospitals in Greece, the larger being the ‘Andreas Sygros’ Hospital for Skin and Venereal Diseases in Athens, and most of the data are obtained from this hospital. Τhe hospital covers a metropolitan area that includes the city of Athens, which is the capital city of Greece, and several other surrounding urban and semi-urban areas, adding up to a population of approximately 4 million, which is almost half the population of Greece. Let also be noted that the hospital admits referrals from other areas, mainly from southern Greece and the islands.
© 2014 European Academy of Dermatology and Venereology
Kanelleas et al.
2
Epidemiological data from both sides of the Atlantic show that primary and secondary syphilis among men who have sex with men (MSM) is on the rise, at least the last decade. Trend data in the United States of America (USA) show that MSM account for nearly three quarters of all cases of primary and secondary syphilis.1 In Europe, almost half (42%) of new syphilis cases reported in 2011 were among MSM, with a broad range from 30% to 70% in different countries.2 Since the vast majority of primary syphilis cases reported to ECDC from Greece originate from our hospital, we conducted an epidemiological study of primary syphilis cases for the period 2005–2012 to investigate the trends of the disease in Greece and whether they are in accordance with the trends in the other European countries and USA. Furthermore, we wanted to investigate the impact of the economic crisis on the population, as far as PS is concerned. More specifically, we aimed to see whether the incidence of primary syphilis is increasing and whether the proportion of MSM among patients is high. We also decided to focus on patients with an HIV (-) status, because we wanted to study syphilis as a single infection and not as a co-infection with HIV.
Materials and methods We reviewed our patients’ records in the Sexually Transmitted Infections Unit of ‘A. Sygros’ Hospital of Skin and Venereal Diseases. Our records are kept electronically. In our search we documented the total annual number of patients, the male to female ratio and the patients’ ethnic origin, sexual orientation and level of education. Higher education level was regarded as hold of at least one university degree. As far as how the diagnosis of PS was established, when a clinical diagnosis of PS was suspected (i.e. when an ulcer or chancre was present), we conducted darkfield microscopic examination of serum obtained from the surface of the chancre. Subsequently, non-treponemal (VDRL) and treponemal (TPHA and ELISA) serological tests were performed in order to confirm the diagnosis.3 Usually both are required to be positive. All patients diagnosed with PS had to be HIV negative, in order to be included in the study. Also, no other apparent STI was present at that time. Data from serological and clinical follow-up were not included complying with the original study design. We analysed our data first on a yearly basis and then we divided our data into two separate groups reflecting two time periods: period A (2005–2008) and period B (2009–2012). We also split our data in three age groups: younger than 30 years old, between 31 and 60 years old and older than 60 years old. Statistical analysis
All categorical variables are described as absolute (n) and relative (%) frequencies. Chi-square test was used in order to compare observed and expected frequencies of PS, while Cochran–Armitage test for trend was used for testing the proportions of patients with PS by year of appearance. All tests were two-sided and con-
JEADV 2014
sidered significant if P < 0.05. AddinsoftTM XLSTAT (XLSTAT, Addinsoft, New York, NY, USA) Version 2013.2.03 statistical software was used for the analysis.
Results We reviewed 1185 patients over the last 8 years from 2005 up to 2012. The total number of patients with PS has risen from 111 in 2005 to 158 in 2012, an increase of 42.3%. The mean annual number is 148. Men clearly outnumber women. The mean male to female ratio is 4.76 : 1, with a peak value of 8.50 : 1 in 2011. Among men, in period A, there were 142 (31.3%) patients younger than 30 years old, 297 (65.6%) between 30 and 60 years old and 14 (3.1%) older than 60 years old, in a total of 453 patients. The respective numbers in period B were 168 (32.8%), 321 (62.6%) and 24 (4.6%), in a total of 513 patients. Within the male patients group, it seems that the number of MSM has risen steadily from 2005 (20.7%) up to 2010 (59.1%), with a decline in 2012 (46.0%). This trend was found statistically significant (P < 0.001). The mean value over 8 years is 45.0% (Fig. 1). Similar findings are discovered when period A (2005– 2008) and period B (2009–2012) are compared. Heterosexual men are the majority in group A (67.77%), while the opposite applies in period B, when MSM are the majority (54.58%). This difference was found statistically significant (P < 0.001) when comparing heterosexual and MSM as a whole (Table 1). In the age group of MSM younger than 30 years old we discovered that the relative number in period B was significantly higher than in period A (70.24% vs. 51.41%) (Table 1). Similar increase in the relative frequencies of MSM is noted in the 31– 60 years old age group. The percentage of MSM almost doubles from period A (24.24%) to period B (49.84%). There is a corresponding decline in the heterosexual men frequency from 75.76% (period A) to 50.16% (period B) (Table 1). In the above 60-year-old age group, there seems to be no difference between the two time periods.
70.0% Homosexual men (%) 60.0% 50.0% 40.0% 30.0% 20.0% 10.0% 0.0% 2005
2006
2007
2008
2009
2010
2011
2012
Figure 1 Relative frequency of men having sex with men (MSM – homosexual) with PS by year of study.
© 2014 European Academy of Dermatology and Venereology
Primary syphilis in Greece
3
Table 1 Comparison of relative frequencies of MSM and heterosexual men within two different time periods Group
2005–2008
2009–2012
Total
P
Men heterosexual
307
233
540
DOI: 10.1111/jdv.12745
ORIGINAL ARTICLE
Primary syphilis in HIV-negative patients is on the rise in Greece: epidemiological data for the period 2005–2012 from a tertiary referral centre in Athens, Greece A. Kanelleas,* C. Stefanaki, I. Stefanaki, G. Bezrondii, V. Paparizos, A. Arapaki, Z. Kripouri, C. Antoniou, E. Nicolaidou 1st Department of Dermatology and Venereology, Sexually Transmitted Infections Unit, University of Athens School of Medicine, ‘A. Sygros’ Hospital, Athens, Greece *Correspondence: A. Kanelleas. E-mail: [email protected]
Abstract Background Epidemiological data on primary syphilis in Greece are limited. Objective The purpose of the present study was to investigate the trends of the disease in Greece during the last few years and whether they are in accordance with the trends in other European countries and the United States of America. Methods We conducted a retrospective analysis based on records of patients who visited the Sexually Transmitted Infections Unit of ‘A. Sygros’ Hospital in Athens, Greece, during the period 2005–2012. Our hospital is a tertiary referral centre for sexually transmitted infections covering an area of more than four million people, which is almost half the population of Greece. We documented the total annual number of patients, the male to female ratio, sexual orientation, patients’ ethnic origin and education level. Results We reviewed the records of 1185 patients with a confirmed diagnosis of primary syphilis. The total number of patients with primary syphilis has risen from 111 in 2005 to 158 in 2012, an increase of 42.3%. The mean annual number is 148. The mean male to female ratio is 4.76 : 1, with a peak value of 8.50 : 1 in 2011. The majority of patients are of Greek origin, ranging from 67.4% to 87.2%. Within the male patients group, it seems that the percentage of men having sex with men has risen steadily from 2005 (20.7%) up to 2010 (59.1%) with a decline in 2012 (46.0%). The mean value over 8 years is 45.0%. Conclusion Primary syphilis in Greece is on the rise. Τhe majority of our patients are Greek, despite immigrant influx. Men clearly outnumber women, representing more than 80% of the total number of patients. Furthermore, there seems to be a trend towards predominance of men having sex with men as the core group among male patients. Received: 21 April 2014; Accepted: 12 August 2014
Conflicts of interest None declared.
Funding sources None declared.
Introduction Syphilis is a sexually transmitted infection (STI) caused by the spirochaeta Treponema pallidum. In most countries of the European Union (EU) and the European Economic Area (EEA), all new cases of primary syphilis (PS) and congenital syphilis are compulsorily reported to national authorities. Then, the European Centre for Disease Control (ECDC) is notified on an annual basis. Unfortunately, not all EU-EEA countries have comprehensive, active and case-based surveillance systems that provide coverage on a national level. The data from Greece that are included in the 2013 Annual Epidemiological Report are based on a passive
JEADV 2014
and aggregated surveillance system that gathers data mainly from STI-dedicated clinics in Skin and Venereal Diseases Hospitals. There are two such hospitals in Greece, the larger being the ‘Andreas Sygros’ Hospital for Skin and Venereal Diseases in Athens, and most of the data are obtained from this hospital. Τhe hospital covers a metropolitan area that includes the city of Athens, which is the capital city of Greece, and several other surrounding urban and semi-urban areas, adding up to a population of approximately 4 million, which is almost half the population of Greece. Let also be noted that the hospital admits referrals from other areas, mainly from southern Greece and the islands.
© 2014 European Academy of Dermatology and Venereology
Kanelleas et al.
2
Epidemiological data from both sides of the Atlantic show that primary and secondary syphilis among men who have sex with men (MSM) is on the rise, at least the last decade. Trend data in the United States of America (USA) show that MSM account for nearly three quarters of all cases of primary and secondary syphilis.1 In Europe, almost half (42%) of new syphilis cases reported in 2011 were among MSM, with a broad range from 30% to 70% in different countries.2 Since the vast majority of primary syphilis cases reported to ECDC from Greece originate from our hospital, we conducted an epidemiological study of primary syphilis cases for the period 2005–2012 to investigate the trends of the disease in Greece and whether they are in accordance with the trends in the other European countries and USA. Furthermore, we wanted to investigate the impact of the economic crisis on the population, as far as PS is concerned. More specifically, we aimed to see whether the incidence of primary syphilis is increasing and whether the proportion of MSM among patients is high. We also decided to focus on patients with an HIV (-) status, because we wanted to study syphilis as a single infection and not as a co-infection with HIV.
Materials and methods We reviewed our patients’ records in the Sexually Transmitted Infections Unit of ‘A. Sygros’ Hospital of Skin and Venereal Diseases. Our records are kept electronically. In our search we documented the total annual number of patients, the male to female ratio and the patients’ ethnic origin, sexual orientation and level of education. Higher education level was regarded as hold of at least one university degree. As far as how the diagnosis of PS was established, when a clinical diagnosis of PS was suspected (i.e. when an ulcer or chancre was present), we conducted darkfield microscopic examination of serum obtained from the surface of the chancre. Subsequently, non-treponemal (VDRL) and treponemal (TPHA and ELISA) serological tests were performed in order to confirm the diagnosis.3 Usually both are required to be positive. All patients diagnosed with PS had to be HIV negative, in order to be included in the study. Also, no other apparent STI was present at that time. Data from serological and clinical follow-up were not included complying with the original study design. We analysed our data first on a yearly basis and then we divided our data into two separate groups reflecting two time periods: period A (2005–2008) and period B (2009–2012). We also split our data in three age groups: younger than 30 years old, between 31 and 60 years old and older than 60 years old. Statistical analysis
All categorical variables are described as absolute (n) and relative (%) frequencies. Chi-square test was used in order to compare observed and expected frequencies of PS, while Cochran–Armitage test for trend was used for testing the proportions of patients with PS by year of appearance. All tests were two-sided and con-
JEADV 2014
sidered significant if P < 0.05. AddinsoftTM XLSTAT (XLSTAT, Addinsoft, New York, NY, USA) Version 2013.2.03 statistical software was used for the analysis.
Results We reviewed 1185 patients over the last 8 years from 2005 up to 2012. The total number of patients with PS has risen from 111 in 2005 to 158 in 2012, an increase of 42.3%. The mean annual number is 148. Men clearly outnumber women. The mean male to female ratio is 4.76 : 1, with a peak value of 8.50 : 1 in 2011. Among men, in period A, there were 142 (31.3%) patients younger than 30 years old, 297 (65.6%) between 30 and 60 years old and 14 (3.1%) older than 60 years old, in a total of 453 patients. The respective numbers in period B were 168 (32.8%), 321 (62.6%) and 24 (4.6%), in a total of 513 patients. Within the male patients group, it seems that the number of MSM has risen steadily from 2005 (20.7%) up to 2010 (59.1%), with a decline in 2012 (46.0%). This trend was found statistically significant (P < 0.001). The mean value over 8 years is 45.0% (Fig. 1). Similar findings are discovered when period A (2005– 2008) and period B (2009–2012) are compared. Heterosexual men are the majority in group A (67.77%), while the opposite applies in period B, when MSM are the majority (54.58%). This difference was found statistically significant (P < 0.001) when comparing heterosexual and MSM as a whole (Table 1). In the age group of MSM younger than 30 years old we discovered that the relative number in period B was significantly higher than in period A (70.24% vs. 51.41%) (Table 1). Similar increase in the relative frequencies of MSM is noted in the 31– 60 years old age group. The percentage of MSM almost doubles from period A (24.24%) to period B (49.84%). There is a corresponding decline in the heterosexual men frequency from 75.76% (period A) to 50.16% (period B) (Table 1). In the above 60-year-old age group, there seems to be no difference between the two time periods.
70.0% Homosexual men (%) 60.0% 50.0% 40.0% 30.0% 20.0% 10.0% 0.0% 2005
2006
2007
2008
2009
2010
2011
2012
Figure 1 Relative frequency of men having sex with men (MSM – homosexual) with PS by year of study.
© 2014 European Academy of Dermatology and Venereology
Primary syphilis in Greece
3
Table 1 Comparison of relative frequencies of MSM and heterosexual men within two different time periods Group
2005–2008
2009–2012
Total
P
Men heterosexual
307
233
540
