- Email: [email protected]
AIDS patients in a tertiary Chinese hospital, Shanghai, China
p u b l i c h e a l t h 1 2 7 ( 2 0 1 3 ) 7 6 e7 8
Available online at www.sciencedirect.com
Public Health journal homepage: www.elsevier.com/puhe
Short Communication
Study on clinical epidemiology of Male HIV/AIDS patients in a tertiary Chinese hospital, Shanghai, China Y. Zheng a, H. Lu a,b,c,*, X. Jiang a, M. Pang d, C. Farthing e a
Shanghai Public Health Clinical Centre, Fudan University, Shanghai, China Huashan Hospital, Fudan University, Shanghai, China c Shanghai Medical College, Fudan University, Shanghai, China d Department of Medicine, Rhode Island Hospital and Brown University School of Medicine, Providence, RI, USA e Merck Sharp & Dohme (Asia) Ltd, Hong Kong, China b
article info Article history: Received 11 May 2011 Received in revised form 24 May 2012 Accepted 24 September 2012 Available online 17 November 2012
Introduction Currently, it is estimated that 740,000 people are living with human immunodeficiency virus (HIV) in China.1e3 In 2011, approximately 28,000 people died from acquired immunodeficiency syndrome (AIDS).2 These numbers must be considered in the context of China’s extremely large population, which is estimated to be approximately 1.3 billion.3 Although China’s HIV epidemic remains of low prevalence overall (0.1% among adults),4 there are pockets of high infection among specific subpopulations, and the danger of the epidemic spreading further into the general population persists.5 This became particularly evident in 2011 when China reported that AIDS had become the country’s leading cause of death among infectious diseases for the first time ever, surpassing both tuberculosis and rabies6. The Shanghai Public Health Clinical Centre is equipped with state-of-the-art facilities and equipment, and provides
clinics, research, training and emergency response. The authors’ department provides comprehensive care for HIV/ AIDS inpatients in Shanghai. It is also an advanced education base for HIV/AIDS care providers of the Chinese Centre for Disease Control and Prevention (CDC). An analysis of basic information on 2320 patients admitted to the Shanghai Public Health Clinical Centre showed that among male AIDS patients, the percentage who acquire HIV by homosexual transmission is growing every year, and the average age of the patients is becoming younger. To help develop more efficient HIV control strategies, a better understanding of the epidemiology of HIV transmission is required in this group of patients. Therefore, this study was planned to examine prevalence and factors associated with HIV infection in men who have sex with men (MSM).
Study population In total, 2320 patients accepted antiretroviral therapy (ART) from October 2005 to September 2012 including 2041 male patients and 279 female patients. In this study, 2041 male patients were investigated.
Study design Information on the time of diagnosis of the patient’s HIV infection, infection routes, time of ART initiation, patient’s age
* Corresponding author. Shanghai Public Health Clinical Centre, Fudan University, No. 2901, Caolang Road, Shanghai 201508, China. Tel./ fax: þ86 021 57248782. E-mail address: [email protected] (H. Lu). 0033-3506/$ e see front matter ª 2012 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.puhe.2012.09.007
77
p u b l i c h e a l t h 1 2 7 ( 2 0 1 3 ) 7 6 e7 8
450 400 350 300 250 200 150 100 50 0
Number
20 05
20 06
Number of homosexual 12 29 transmitted patients Percentage in male 38.71 34.94 patients(%)
20 07
20 08
20 09
20 10
20 11
20 12
36
72
125
228
388
325
45
80 70 60 50 40 % 30 20 10 0
49.65 50.81 60.64 64.03 68.57
Fig. 1 e The number of homosexual transmitted HIV infections and percentage in male patients in calendar years.
and marital status was collated, as well as whether their spouse was infected with HIV. Patients were divided into two groups according to MSM and heterosexual behaviour. Variations in age, marital status, education level, and time between diagnosis of HIV infection and initiation of ART were compared between these two groups.
Statistical analysis Data are presented as mean standard error of the mean for each group. Statistical Package for the Social Sciences Version 15.0 (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. The differences between the two groups were determined using Student’s t-test. P < 0.05 was taken to indicate significance.
Results Among 2041 male patients with AIDS, 1215 patients were infected through MSM behaviour (59.53%). The numbers and percentages of male patients that were MSM in each calender year is depicted in Fig. 1. Patients in the MSM group initiated ART at younger age (36.10 10.84 years old), compared with
patients in the heterosexual group (45.83 11.12) (p < 0.01). Regarding marital status, there were 778 (64.03%) unmarried patients in the MSM group versus 164 (19.85%) patients in heterosexual group. In both groups, there were spousal infections 10 in the MSM group (2.29% of married patients), and 67 in the heterosexual group (10.12% of married patients). There were significant differences in the educational level between the two groups. 757 (62.30%) patients in the MSMl group had bachelor or higher level degrees, whereas only 104 (12.59%) patients in the heterosexual group had the same level of education. Detailed data is listed in Table 1.
Discussion With the growth of the HIV epidemic in China, HIV transmission routes are gradually changing from mainly intravenous drug use, blood transfusion and plasma donation to sexual transmission. A significant increase in HIV infection has been observed amongst MSM, especially in the more economically developed areas. The percentage of HIV infection mediated by MSM behaviour has increased every year, and is currently the major route of infection in male patients. More attention and effective measures are needed to prevent HIV spreading in this high-risk group.
Table 1 e Comparison of factors in homosexual and heterosexual transmission group. Number (n)
Homosexual group Non-homosexual group t p
Age at initiation of treatment (years)
Marriage status [n(%)] Unmarried
Married (including divorced, widowhood)
Infection of spouse in married patients [n (percentage in married patients %)]
Education [n(%)] College or above
1215
36.10 10.84
778 (64.03)
437 (35.97)
10 (2.29)
757 (62.30)
826
45.83 11.12
164 (19.85)
662 (80.15)
67 (10.12)
104 (12.59)
12.786 0.000
78
p u b l i c h e a l t h 1 2 7 ( 2 0 1 3 ) 7 6 e7 8
International studies indicate that unprotected anal intercourse is the major route of transmission amongst MSM.7e9 Although HIV infection affects less than 1% of the general population in China, and less than 5% of female sex workers, 21% of MSM are infected and this percentage is increasing at 5% per year,10 with an average age of 37 (22e63) years.11 Other studies suggest that 25% of MSM in China have HIV infection.12 According to a report from the Chinese CDC in 20115, 62.6% of HIV infections were transmitted through heterosexual behaviour, and 13.7% were transmitted through MSM behaviour with an increasing trend. However, the latter value could be an underestimate as many MSM are unwilling to reveal their true risk group status. In more economically developed areas such as Shanghai, the percentage of MSM-transmitted cases of HIV infection is significantly higher than the national average, and increased from 38.71% in 2005 to 68.57% in 2012 in male patients; The average age of the MSM patients was much lower than the age of the heterosexual patients, and higher education levels were observed in the MSM patients compared with the heterosexual patients. The rapid rise in this group raises concern about the possibility of a major HIV/AIDS epidemic in China, with much higher percentages of the general population being affected than is currently the case. Urgent measures need to be taken for effective prevention in the MSM community. This study found that 35.97% of MSM patients were married with female spouses. These data indicate that their sexual orientation has not been recognized by society, and they feel they have to be married due to the pressure of a traditional culture. This increases the chance of HIV transmission to their spouses. Attention should be paid to their marital status and the possibility of spousal infection in their spouse. Given the seriousness of HIV infection rates and their rapid increase amongst MSM, more efficient strategies including advocacy of safer sex behaviour and earlier HIV testing should be employed. Consideration should perhaps be given to adopting a treatment for prevention approach to the MSM population, with widespread HIV testing and treatment of all positives regardless of CD4 count. This would need to be done with great sensitivity, and with the active participation of MSM groups and the absolute avoidance of any coercion. Another strategy that could be considered is pre-exposure prophylaxis, which has recently been shown to be successful in clinical trials. With one in five individuals in the world living in China, it is critical that the country continues with its efforts to prevent a generalized epidemic by raising awareness and reducing infections in the current high prevalence groups of injecting drug users, former plasma donors and MSM.
Acknowledgement Ethical approval Ethical approval for data collection was gained from the Ethic Committee of Shanghai Public Health Clinical Center,
2901 Cao Lang Road, Jinshan District, Shanghai, 201508, China
Funding This study was support by the following grants: 1. “Technological platform of clinical evaluation of anti-retroviral drugs”, Chinese key projects on new drugs from State Council of China (2012ZX09303-013); 2. “The promotion and optimization of standardized treatment strategies of patients co-infected with HIV tuberculosis”, Chinese Twelfth Five Key projects on infectious diseases from Chinese Ministry of Health (2012ZX10001003-002).
Competing interests None declared.
references
1. UNAIDS. UNAIDS report on the global AIDS epidemic; 2010. 2. Chow EP, Wilson DP, Zhang L. The next era of HIV in China: rapidly spreading epidemics among men who have sex with men. J Acquir Immune Defic Syndr 2010;55:e32e3. 3. CIA. CIA world factbook: China; 2010. 4. van Griensven F, de Lind van Wijngaarden JW. A review of the epidemiology of HIV infection and prevention responses among MSM in Asia. AIDS 2010;24(Suppl. 3):S30e40. 5. Chinese Center for Disease Control and Prevention. Available at: http://www.chinacdc.cn/ (accessed October 2012). 6. Ministry of Health of the People’s Republic of China. Available at: http://www.moh.gov.cn/publicfiles/business/htmlfiles/ wsb/index.htm (accessed October 2012). 7. Darrow WW, Jaffe HW, Curran JW. Passive anal intercourse as a risk factor for AIDS in homosexual men[J]. Lancet 1983;2:160. 8. Detels R, Fahey JL, Schwartz K, Greene RS, Visscher BR, Gottlieb MS. Relation between sexual practices and T-cell subsets in homosexually active men[J]. Lancet 1983;1:609e11. 9. Mayer KH, Ayotte D, Groopman JE, Stoddard AM, Sarngadharan M, Gallo R. Association of human T lymphotropic virus type III antibodies with sexual and other behaviors in a cohort of homosexual men from Boston with and without generalized lymphadenopathy. Am J Med 1986;80:357e63. 10. Sanchez J, Lama JR, Kusunoki L, Manrique H, Goicochea P, Lucchetti A, et al. HIV-1, sexually transmitted infections, and sexual behavior trends among men who have sex with men in Lima, Peru. J Acquir Immune Defic Syndr 2007;44:578e85. 11. Jin F, Crawford J, Garrett P. HIV risk reduction behaviours in gay men: unprotected anal intercourse, risk reduction behaviours, and subsequent HIV infection in a cohort of homosexual men. AIDS 2009;23:243e52. 12. Centers for Disease Control and Prevention. HIV prevalence, unrecognized infection, and HIV testing among men who have sex with mendfive US cities, Jun 2004eApril 2005. MMWR Morb Mortal Wkly Rep 2005;54:597e601.
Available online at www.sciencedirect.com
Public Health journal homepage: www.elsevier.com/puhe
Short Communication
Study on clinical epidemiology of Male HIV/AIDS patients in a tertiary Chinese hospital, Shanghai, China Y. Zheng a, H. Lu a,b,c,*, X. Jiang a, M. Pang d, C. Farthing e a
Shanghai Public Health Clinical Centre, Fudan University, Shanghai, China Huashan Hospital, Fudan University, Shanghai, China c Shanghai Medical College, Fudan University, Shanghai, China d Department of Medicine, Rhode Island Hospital and Brown University School of Medicine, Providence, RI, USA e Merck Sharp & Dohme (Asia) Ltd, Hong Kong, China b
article info Article history: Received 11 May 2011 Received in revised form 24 May 2012 Accepted 24 September 2012 Available online 17 November 2012
Introduction Currently, it is estimated that 740,000 people are living with human immunodeficiency virus (HIV) in China.1e3 In 2011, approximately 28,000 people died from acquired immunodeficiency syndrome (AIDS).2 These numbers must be considered in the context of China’s extremely large population, which is estimated to be approximately 1.3 billion.3 Although China’s HIV epidemic remains of low prevalence overall (0.1% among adults),4 there are pockets of high infection among specific subpopulations, and the danger of the epidemic spreading further into the general population persists.5 This became particularly evident in 2011 when China reported that AIDS had become the country’s leading cause of death among infectious diseases for the first time ever, surpassing both tuberculosis and rabies6. The Shanghai Public Health Clinical Centre is equipped with state-of-the-art facilities and equipment, and provides
clinics, research, training and emergency response. The authors’ department provides comprehensive care for HIV/ AIDS inpatients in Shanghai. It is also an advanced education base for HIV/AIDS care providers of the Chinese Centre for Disease Control and Prevention (CDC). An analysis of basic information on 2320 patients admitted to the Shanghai Public Health Clinical Centre showed that among male AIDS patients, the percentage who acquire HIV by homosexual transmission is growing every year, and the average age of the patients is becoming younger. To help develop more efficient HIV control strategies, a better understanding of the epidemiology of HIV transmission is required in this group of patients. Therefore, this study was planned to examine prevalence and factors associated with HIV infection in men who have sex with men (MSM).
Study population In total, 2320 patients accepted antiretroviral therapy (ART) from October 2005 to September 2012 including 2041 male patients and 279 female patients. In this study, 2041 male patients were investigated.
Study design Information on the time of diagnosis of the patient’s HIV infection, infection routes, time of ART initiation, patient’s age
* Corresponding author. Shanghai Public Health Clinical Centre, Fudan University, No. 2901, Caolang Road, Shanghai 201508, China. Tel./ fax: þ86 021 57248782. E-mail address: [email protected] (H. Lu). 0033-3506/$ e see front matter ª 2012 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.puhe.2012.09.007
77
p u b l i c h e a l t h 1 2 7 ( 2 0 1 3 ) 7 6 e7 8
450 400 350 300 250 200 150 100 50 0
Number
20 05
20 06
Number of homosexual 12 29 transmitted patients Percentage in male 38.71 34.94 patients(%)
20 07
20 08
20 09
20 10
20 11
20 12
36
72
125
228
388
325
45
80 70 60 50 40 % 30 20 10 0
49.65 50.81 60.64 64.03 68.57
Fig. 1 e The number of homosexual transmitted HIV infections and percentage in male patients in calendar years.
and marital status was collated, as well as whether their spouse was infected with HIV. Patients were divided into two groups according to MSM and heterosexual behaviour. Variations in age, marital status, education level, and time between diagnosis of HIV infection and initiation of ART were compared between these two groups.
Statistical analysis Data are presented as mean standard error of the mean for each group. Statistical Package for the Social Sciences Version 15.0 (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. The differences between the two groups were determined using Student’s t-test. P < 0.05 was taken to indicate significance.
Results Among 2041 male patients with AIDS, 1215 patients were infected through MSM behaviour (59.53%). The numbers and percentages of male patients that were MSM in each calender year is depicted in Fig. 1. Patients in the MSM group initiated ART at younger age (36.10 10.84 years old), compared with
patients in the heterosexual group (45.83 11.12) (p < 0.01). Regarding marital status, there were 778 (64.03%) unmarried patients in the MSM group versus 164 (19.85%) patients in heterosexual group. In both groups, there were spousal infections 10 in the MSM group (2.29% of married patients), and 67 in the heterosexual group (10.12% of married patients). There were significant differences in the educational level between the two groups. 757 (62.30%) patients in the MSMl group had bachelor or higher level degrees, whereas only 104 (12.59%) patients in the heterosexual group had the same level of education. Detailed data is listed in Table 1.
Discussion With the growth of the HIV epidemic in China, HIV transmission routes are gradually changing from mainly intravenous drug use, blood transfusion and plasma donation to sexual transmission. A significant increase in HIV infection has been observed amongst MSM, especially in the more economically developed areas. The percentage of HIV infection mediated by MSM behaviour has increased every year, and is currently the major route of infection in male patients. More attention and effective measures are needed to prevent HIV spreading in this high-risk group.
Table 1 e Comparison of factors in homosexual and heterosexual transmission group. Number (n)
Homosexual group Non-homosexual group t p
Age at initiation of treatment (years)
Marriage status [n(%)] Unmarried
Married (including divorced, widowhood)
Infection of spouse in married patients [n (percentage in married patients %)]
Education [n(%)] College or above
1215
36.10 10.84
778 (64.03)
437 (35.97)
10 (2.29)
757 (62.30)
826
45.83 11.12
164 (19.85)
662 (80.15)
67 (10.12)
104 (12.59)
12.786 0.000
78
p u b l i c h e a l t h 1 2 7 ( 2 0 1 3 ) 7 6 e7 8
International studies indicate that unprotected anal intercourse is the major route of transmission amongst MSM.7e9 Although HIV infection affects less than 1% of the general population in China, and less than 5% of female sex workers, 21% of MSM are infected and this percentage is increasing at 5% per year,10 with an average age of 37 (22e63) years.11 Other studies suggest that 25% of MSM in China have HIV infection.12 According to a report from the Chinese CDC in 20115, 62.6% of HIV infections were transmitted through heterosexual behaviour, and 13.7% were transmitted through MSM behaviour with an increasing trend. However, the latter value could be an underestimate as many MSM are unwilling to reveal their true risk group status. In more economically developed areas such as Shanghai, the percentage of MSM-transmitted cases of HIV infection is significantly higher than the national average, and increased from 38.71% in 2005 to 68.57% in 2012 in male patients; The average age of the MSM patients was much lower than the age of the heterosexual patients, and higher education levels were observed in the MSM patients compared with the heterosexual patients. The rapid rise in this group raises concern about the possibility of a major HIV/AIDS epidemic in China, with much higher percentages of the general population being affected than is currently the case. Urgent measures need to be taken for effective prevention in the MSM community. This study found that 35.97% of MSM patients were married with female spouses. These data indicate that their sexual orientation has not been recognized by society, and they feel they have to be married due to the pressure of a traditional culture. This increases the chance of HIV transmission to their spouses. Attention should be paid to their marital status and the possibility of spousal infection in their spouse. Given the seriousness of HIV infection rates and their rapid increase amongst MSM, more efficient strategies including advocacy of safer sex behaviour and earlier HIV testing should be employed. Consideration should perhaps be given to adopting a treatment for prevention approach to the MSM population, with widespread HIV testing and treatment of all positives regardless of CD4 count. This would need to be done with great sensitivity, and with the active participation of MSM groups and the absolute avoidance of any coercion. Another strategy that could be considered is pre-exposure prophylaxis, which has recently been shown to be successful in clinical trials. With one in five individuals in the world living in China, it is critical that the country continues with its efforts to prevent a generalized epidemic by raising awareness and reducing infections in the current high prevalence groups of injecting drug users, former plasma donors and MSM.
Acknowledgement Ethical approval Ethical approval for data collection was gained from the Ethic Committee of Shanghai Public Health Clinical Center,
2901 Cao Lang Road, Jinshan District, Shanghai, 201508, China
Funding This study was support by the following grants: 1. “Technological platform of clinical evaluation of anti-retroviral drugs”, Chinese key projects on new drugs from State Council of China (2012ZX09303-013); 2. “The promotion and optimization of standardized treatment strategies of patients co-infected with HIV tuberculosis”, Chinese Twelfth Five Key projects on infectious diseases from Chinese Ministry of Health (2012ZX10001003-002).
Competing interests None declared.
references
1. UNAIDS. UNAIDS report on the global AIDS epidemic; 2010. 2. Chow EP, Wilson DP, Zhang L. The next era of HIV in China: rapidly spreading epidemics among men who have sex with men. J Acquir Immune Defic Syndr 2010;55:e32e3. 3. CIA. CIA world factbook: China; 2010. 4. van Griensven F, de Lind van Wijngaarden JW. A review of the epidemiology of HIV infection and prevention responses among MSM in Asia. AIDS 2010;24(Suppl. 3):S30e40. 5. Chinese Center for Disease Control and Prevention. Available at: http://www.chinacdc.cn/ (accessed October 2012). 6. Ministry of Health of the People’s Republic of China. Available at: http://www.moh.gov.cn/publicfiles/business/htmlfiles/ wsb/index.htm (accessed October 2012). 7. Darrow WW, Jaffe HW, Curran JW. Passive anal intercourse as a risk factor for AIDS in homosexual men[J]. Lancet 1983;2:160. 8. Detels R, Fahey JL, Schwartz K, Greene RS, Visscher BR, Gottlieb MS. Relation between sexual practices and T-cell subsets in homosexually active men[J]. Lancet 1983;1:609e11. 9. Mayer KH, Ayotte D, Groopman JE, Stoddard AM, Sarngadharan M, Gallo R. Association of human T lymphotropic virus type III antibodies with sexual and other behaviors in a cohort of homosexual men from Boston with and without generalized lymphadenopathy. Am J Med 1986;80:357e63. 10. Sanchez J, Lama JR, Kusunoki L, Manrique H, Goicochea P, Lucchetti A, et al. HIV-1, sexually transmitted infections, and sexual behavior trends among men who have sex with men in Lima, Peru. J Acquir Immune Defic Syndr 2007;44:578e85. 11. Jin F, Crawford J, Garrett P. HIV risk reduction behaviours in gay men: unprotected anal intercourse, risk reduction behaviours, and subsequent HIV infection in a cohort of homosexual men. AIDS 2009;23:243e52. 12. Centers for Disease Control and Prevention. HIV prevalence, unrecognized infection, and HIV testing among men who have sex with mendfive US cities, Jun 2004eApril 2005. MMWR Morb Mortal Wkly Rep 2005;54:597e601.