- Email: [email protected]
Concentrated epidemics of HIV, HCV, and HBV among Afghan refugees
434
Letters to the Editor population of Afghan refugees in any single country, are residing in Pakistan.1 These refugees reside both in camps and urban slums, struggling against impoverishment, overcrowding, poor sanitation, lack of clean water, and of healthcare infrastructure.2,3 Human Immunodeficiency, Hepatitis B and C viruses (respectively, HIV, HCV, and HBV) share similar modes of transmission, that include blood to blood contact, sexual contact with infected person or vertical transmission (mother to child). Pakistan has an overall HIV prevalence of 0.1%, but within certain high risk groups, such as IDUs and MSM, concentrated HIV epidemics exist.4e6 According to a study which reviewed medical and public health literature regarding Hepatitis B and C in Pakistan, prevalence of 2.4 and 3%, respectively, were reported for the general population.7 Limited data exist on the prevalence of HIV, HCV and HBV in Afghanistan8e12 whereas no reports exist on the prevalence of these infections among Afghan refugees. As in other vulnerable populations, Injection drug users (IDUs), males who have sex with males (MSM), commercial sex workers, migrant workers and prisoners, are recognized as subgroups at high risk of the said infections among
*Corresponding author. Department of Infectious Diseases, Asan Medical Center, University of Ulsan College of Medicine, 86, Asanbyeongwon-gil, Songpa-gu, Seoul 138-736, Republic of Korea. Tel.: þ82 2 3010 3305; fax: þ82 3010 6970. E-mail address: [email protected] (S.-H. Kim) 31 August 2010 Available online 8 September 2010 ª 2010 The British Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jinf.2010.08.011
Concentrated epidemics of HIV, HCV, and HBV among Afghan refugees According to a 2007 United Nations High Commissioner for Refugees (UNHCR) report, 1.9 million, the largest
Table 1
Demographic details of study participants.
Categories
Total Z 556
HIV
HCV
Gender Males Females
410(73.7%) 146(26.2%)
33*(8.04%) 0*
167*(40.7%) 38*(26.0%)
40(9.75%) 11(7.53%)
Location Karachi Quetta
530(95.3%) 26(4.67%)
25*(4.71%) 8*(30.7%)
192(36.2%) 13(50.0%)
48(9.05%) 3(11.5%)
Marital Status Married Single Widow Unknown
443(79.6%) 107(19.2%) 1(0.17%) 5(0.89%)
27(6.09%) 6(5.60%)
169(38.1%) 35(32.7%) 1(100%)
45(10.1%) 6(5.60%)
Age Groups 10e19 years 20e29 years 30e39 years 40e49 years 50e59 years 60 and up Unknown
44(7.91%) 193(34.7%) 161(28.9%) 125(22.4%) 18(3.23%) 13(2.33%) 2(0.35%)
Profession Homemaker Driver Shop Keeper Student Guard Factory Hotel/Tea shop Other Labor/Loader/worker Unknown
69(12.4%) 50(8.99%) 91(16.3%) 38(6.83%) 35(6.29%) 29(5.21%) 21(3.77%) 80(14.3%) 70(12.5%) 73(13.1%)
0 0
0
HBV
0 0
3(6.81%) 14(7.25%) 11(6.83%) 5(4.00%)
9*(20.4%) 63(32.6%) 61(37.8%) 55(44.0%) 7(38.8%) 9*(69.2%) 1(50.0%)
3(6.81%) 14(7.25%) 12(7.45%) 18*(14.4%) 3(16.6%) 1(7.69%) 0
0* 6*(12.0%) 11*(12.0%) 2(5.26%) 1(2.85%) 0 4*(19.0%) 1(1.25%) 2(2.85%) 6(8.21%)
18*(26.0%) 20(40.0%) 37(40.6%) 7*(18.4%) 18(51.4%) 16(55.1%) 11(52.3%) 37(46.2%) 23(32.8%) 18(24.6%)
5(7.24%) 2(4.00%) 6(6.59%) 3(7.89%) 2(5.71%) 11*(37.9%) 1(4.76%) 7(8.75%) 6(8.57%) 8(10.9%)
0 0 0
The frequencies of all values are given in parentheses. *The association of demographics with HIV, HCV or HBV significant (p 0.05) calculated through Pearson Chi square test.
Letters to the Editor
435
the Afghan native12 and refugee populations.1,13,14 Following an analysis of HIV, HCV, and HBV among the Afghan refugees residing in Pakistan, we report here the existence of concentrated epidemics of all three infections in the refugee population. Samples were obtained through ‘Convenience Sampling’ of subjects attending antenatal clinics and persons participating in free health camps organized by the Infection Control Society, Pakistan, for screening of Hepatitis B, C and HIV, and for HBV vaccination. A total of 556 blood samples were collected from Afghan refugees. An informed consent was obtained from the study participants, and a questionnaire was administered to determine high risk behavior, prior to the collection of blood samples. The study was approved by the Ethical Review Committee, Aga Khan University, Karachi, Pakistan. Sera specimens were collected from the study subjects and Enzyme Linked Immuno Sorbent Assay (ELISA) was performed to check antibodies against HIV1/2 and HCV using Bioelisa HIV-1 þ 2 (rec) and Bioelisa HCV 4.0, respectively. Surface antigen against HBV was detected using Bioelisa HBsAg colour. For positive samples, results were confirmed twice using the same ELISA kits. Blood samples were collected from 556 participants. The majority of which came from various parts of Karachi (n Z 530) and a few from Quetta (n Z 26). The study group comprised mostly of males (73.7%) and most of the participants (34.7%) belonged to the age groups 20e29, representing a diversity of professions (Table 1). High risk behaviors such as drug use, injecting drugs and traveling abroad were observed in a considerable number of refugees (Tables 1 and 2). Out of 556 samples, 33 (5.93%) were found
Table 2
positive for anti-HIV antibodies, 205 (36.8%) for anti-HCV antibodies and 51 (9.17%) for Hepatitis B surface antigen. A total of 11 (1.97%) study subjects had HIV infection alone, 164 (29.4%) were infected only with HCV, whereas 30 (5.39%) were infected with HBV alone. 20 subjects (3.59%) were found to be co-infected with HCV and HIV, 19 (3.41%) had HCV and HBV, whereas 2 individuals (0.35%) carried all three viruses. Our study on the seroprevalence of HIV, HCV and HBV viruses among Afghan refugees in Pakistan revealed a higher occurrence of these viruses in the said group as compared to the general population of Pakistan. Risk factors possibly associated with these infections were drug abuse, transmigration, and, unsafe sexual behavior. A major high risk behavior observed among infected participants in this study was drug abuse (28.4%). Out of these drug users, some individuals reported the use of only injecting drugs (12.8%) while others stated to both smoking/inhaling as well as injecting drugs (18.5%). A significant correlation was observed between drug use and HIV infection in our study subjects (Table 2). In Afghanistan, opium and heroin have been used traditionally as medicine and for recreation. A study comparing the risk behaviors of Afghans and Pakistanis reports that Afghans are more likely than Pakistanis to have injected drugs, used opiate as their first illicit drug, report needle-sharing, or have a drug user in their family.15 Compared to the Pakistanis, Afghans have been reported to have lower awareness of HIV/AIDS.15 We observed a high prevalence of HIV (5.93%) in our study; very few participants, however, admitted to having multiple sex partners or contact with sex workers. In this group this may be
Correlation of viral infections with high risk behaviors.
Categories
Total Z 556
HIV
HCV
Drug Abuse Total Drug Abuse Only Smoked/Inhaled drugs Only Injected drugs Smoked/Inhaled þ Injected drugs
130(23.3%) 88(15.8%) 20(3.59%) 22(3.95%)
14*(10.7%) 6(6.81%) 2(10.0%) 6*(27.2%)
59*(45.3%) 40(45.4%) 7(35.0%) 12(54.5%)
Sexual History Homosexuality Multiple sex partners Travel History Total Travel History Abroad Afghanistan Saudi Arabia Sudan U.A.E. Afghanistan þ India Afghanistan þ Iran Afghanistan þ Saudi Arabia Afghanistan þ South Africa Afghanistan þ U.A.E. Others
6(1.07%) 2(0.35%) 260(46.7%) 214(38.4%) 6(1.07%) 1(0.17%) 17(3.05%) 1(0.17%) 1(0.17%) 3(0.53%) 5(0.89%) 6(1.07%) 6(1.07%)
0 2*(100%) 12(4.61%) 9(4.20%) 0 0 1(5.88%) 0 1*(100%) 0 1(20.0%) 0 0
3(50.0%) 2(100%) 78*(30.0%) 53*(24.7%) 4(66.6%) 1(100%) 10(58.8%) 1(100%) 1(100%) 1(33.3%) 4*(80.0%) 2(33.3%) 1(16.6%)
HBV 9(6.9%) 6(6.81%) 2(10.0%) 1(4.54%) 0 0 15*(5.76%) 11*(5.14%) 0 0 4*(23.5%) 0 0 0 0 0 0
The frequencies of all values are given in parentheses. *The association of high risk behavior with HIV, HCV or HBV significant (p 0.05) calculated through Pearson Chi square test.
436 attributed to social taboos regarding sexual matters.16 Frequent travel is also regarded as high risk behavior toward the spread of viral and other infections.14,17,18 Of those individuals who were infected in our study group, 27.2% travelled to Afghanistan (some made multiple visits), 5.69% visited the UAE and 1.62% went to Saudi Arabia. Statistical analysis revealed a strong correlation between travel to Afghanistan and infections with all three viruses (Table 2). Previously we have reported that Pakistanis who had travelled abroad and overseas contract workers, especially in the UAE countries, were potential source of concentrated HIV epidemics in Pakistan.19 This highlights a need for focused immigration policies that incorporate prevention and awareness programs for sexually-transmitted and blood-borne infections among refugees, migrant workers and travelers. In addition to single infections, we also observed coinfections in our study. Dually infected HIV patients are known to have unfavorable prognosis, both in the case of HIVeHCV20 as well as HIVeHBV21,22 combinations. While such individuals will need specially tailored treatment and management protocols, particular attention must be paid to timely diagnosis and to the control of high risk behaviors which can prevent the occurrence of multiple infections in the first place. Harm reduction programs for high risk groups are in place in Afghanistan23 as well as in Pakistan.24,25 The elevated incidence of viral infections in the Afghan refugee population reported here, however, highlights the need for the implementation of such programs especially targeted toward control and prevention of sexually-transmitted and blood-borne infections in this particular high group.
Funding support This study was partly funded by the Higher Education Commission, Pakistan, grant 20-775, and Pakistan Science Foundation, Pakistan, grant 232.
Conflict of interest None.
References 1. Rajabali A, Moin O, Ansari AS, Khanani MR, Ali SH. Communicable disease among displaced Afghans: refuge without shelter. Nat Rev Microbiol 2009;7(8):609e14. 2. Connolly MA, Gayer M, Ryan MJ, Salama P, Spiegel P, Heymann DL. Communicable diseases in complex emergencies: impact and challenges. Lancet 2004;364(9449): 1974e83. 3. Beckwith CG, DeLong AK, Desjardins SF, Gillani F, Bazerman L, Mitty JA, et al. HIV infection in refugees: a case-control analysis of refugees in Rhode Island. Int J Infect Dis 2009;13 (2):186e92. 4. Surveillance Data. Sindh AIDS Control Program. In: Government of Sindh Pakistan, editor. 2004. 5. Shah SA, Altaf A, Mujeeb SA, Memon A. An outbreak of HIV infection among injection drug users in a small town in Pakistan: potential for national implications. Int J STD AIDS 2004;15(3): 209.
Letters to the Editor 6. WHO/UNAIDS/UNICEF. Epidemiological Fact Sheet on HIV and AIDS Core data on epidemiology and response Pakistan. 2008; Update. 7. Ali SA, Donahue RM, Qureshi H, Vermund SH. Hepatitis B and hepatitis C in Pakistan: prevalence and risk factors. Int J Infect Dis 2009;13(1):9e19. 8. Todd CS, Abed AM, Strathdee SA, Scott PT, Botros BA, Safi N, et al. HIV, hepatitis C, and hepatitis B infections and associated risk behavior in injection drug users, Kabul, Afghanistan. Emerg Infect Dis 2007;13(9):1327e31. 9. Todd CS, Nasir A, Stanekzai MR, Bautista CT, Botros BA, Scott PT, et al. HIV, hepatitis B, and hepatitis C prevalence and associated risk behaviors among female sex workers in three Afghan cities. AIDS 2010;24(Suppl. 2):S69e75. 10. Todd CS, Ahmadzai M, Atiqzai F, Smith JM, Miller S, Azfar P, et al. Prevalence and correlates of HIV, syphilis, and hepatitis knowledge among intrapartum patients and health care providers in Kabul, Afghanistan. AIDS Care 2009;21(1): 109e17. 11. Todd CS, Ahmadzai M, Atiqzai F, Miller S, Smith JM, Ghazanfar SA, et al. Seroprevalence and correlates of HIV, syphilis, and hepatitis B and C virus among intrapartum patients in Kabul, Afghanistan. BMC Infect Dis 2008; 8:119. 12. UNGASS country progress report Afghanistan National AIDS Control Program, http://data.unaids.org/pub/Report/2010/afghanistan_ 2010_country_progress_report_en.pdf; August 30 2010. 13. Adoga MP, Banwat EB, Forbi JC, Nimzing L, Pam CR, Gyar SD, et al. Human immunonodeficiency virus, hepatitis B virus and hepatitis C virus: sero-prevalence, co-infection and risk factors among prison inmates in Nasarawa State, Nigeria. J Infect Dev Ctries 2009;3(7):539e47. 14. Khan S, Rai MA, Khanani MR, Khan MN, Ali SH. HIV-1 subtype A infection in a community of intravenous drug users in Pakistan. BMC Infect Dis 2006;6:164. 15. Zafar T, Brahmbhatt H, Imam G, ul Hassan S, Strathdee SA. HIV knowledge and risk behaviors among Pakistani and Afghani drug users in Quetta, Pakistan. J Acquir Immune Defic Syndr 2003;32(4):394e8. 16. Shafiq M, Ali SH. Sexually transmitted infections in Pakistan. Lancet Infect Dis 2006;6(6):321e2. 17. Resurgence of wild poliovirus type 1 transmission and consequences of importatione21 countries, 2002e2005. MMWR Morb Mortal Wkly Rep 2006;55(6):145e50. 18. Kazmi JH, Pandit K. Disease and dislocation: the impact of refugee movements on the geography of malaria in NWFP, Pakistan. Soc Sci Med 2001;52(7):1043e55. 19. Baqi S, Kayani N, Khan JA. Epidemiology and clinical profile of HIV/AIDS in Pakistan. Trop Doct 1999;29(3):144e8. 20. CDC. Hepatitis C virus and HIV coinfection. IDU HIV Prevention [cited; Available from: http://www.cdc.gov/IDU/hepatitis/ hepc_and_hiv_co.pdf; September 2002. 21. Dore GJ, Cooper DA. The impact of HIV therapy on co-infection with hepatitis B and hepatitis C viruses. Curr Opin Infect Dis 2001;14(6):749e55. 22. Soriano V on behalf of the SMART-INSIGHT study group. Antiretroviral therapy re-initiation and HBV rebound among HIV-HBV coinfected patients following ART interruption in the SMART Study. 16th Conference on Retroviruses and Opportunistic Infections, Montreal, February 2009. [Abstr. Q-111]. 23. Todd CS, Stibich MA, Stanekzai MR, Rasuli MZ, Bayan S, Wardak SR, et al. A qualitative assessment of injection drug use and harm reduction programmes in Kabul, Afghanistan: 2006e2007. Int J Drug Policy 2009;20(2):111e20. 24. Altaf A, Shah SA, Zaidi NA, Memon A, Nadeem ur R, Wray N. High risk behaviors of injection drug users registered with harm reduction programme in Karachi, Pakistan. Harm Reduct J 2007;4:7.
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25. Emmanuel F, Fatima M. Coverage to curb the emerging HIV epidemic among injecting drug users in Pakistan: delivering prevention services where most needed. Int J Drug Policy 2008;19 (Suppl. 1):S59e64.
Muhammad Rafiq Khanania Department of Microbiology, Dow University of Health Sciences, Karachi, Pakistan Amna S. Ansaria Saeed Khan Mehreen Somani Department of Biological and Biomedical Sciences, Aga Khan University, Karachi, Pakistan Shahana Urooj Kazmi Department of Microbiology, University of Karachi, Pakistan Syed H. Ali* Department of Biological and Biomedical Sciences, Aga Khan University, P.O. Box 3500, Karachi 74800, Pakistan Department of Microbiology, Dow University of Health Sciences, Karachi, Pakistan *Corresponding author. Tel.: +92 21 486 4433. E-mail address: [email protected] 30 August 2010 Available online 8 September 2010 ª 2010 The British Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jinf.2010.08.009
Pandemic (H1N1) 2009 influenza in HIV-infected adults: Clinical features, severity, and outcome
Dear Editor, We read with interest the paper by Redelman-Sidi et al. on 2009 H1N1 influenza infection in patients with cancer and hematopoietic stem cell transplant, reporting that these immunosuppressed patients did not have substantial risk for poor outcome from pH1N1.1 In April 2009, the World Health Organization was alerted of human infections with the novel pandemic (H1N1) 2009 (pH1N1) virus. The virus continues to spread globally.2 In Singapore, pH1N1 was first detected on May 26, 2009,3 in a returning student from New York. Rapid transmission occurred, despite containment measures.4,5 Although usually mild, pH1N1 can cause hospitalization in 2e5% of cases, and increase risk of complications in immunosuppressed persons.6e9 In HIV-positive individuals, a
MRK and ASA have equally contributed to this study.
pH1N1 fatalities have been reported.10e12 Although influenza has been described to cause significant morbidity and mortality among HIV-positive patients,13e18 the impact of pH1N1 on HIV-positive individuals is not well understood.10e12,19 To understand the epidemiological and clinical features, illness severity, and clinical outcomes of pH1N1 infection in HIV-positive adults, we conducted a matched case-control study at the Communicable Disease Centre at Tan Tock Seng Hospital Singapore, from July 1 to September 30, 2009. Case patients were HIV-positive adults who were confirmed with pH1N1 infection by polymerase chain reaction assay on respiratory specimens. Two control groups were randomly selected from adults confirmed with pH1N1 during the same period, but without a positive HIV status. Control group 1 (CG1) consisted of patients with at least one underlying medical condition other than HIV. Control group 2 (CG2) comprised those without any co-morbidity. Each HIV-patient was compared with 3 controls in each control group respectively, matched for age and hospitalization status (Table 1). Casenotes were reviewed for demographic and epidemiologic characteristics, pre-existing medical conditions, clinical signs and symptoms, haematological and biochemical markers, microbiological and radiological findings, treatment, and clinical outcomes. Eleven HIV-positive patients with pH1N1 were identified. Their median CD4 count was 223 cells/uL (range 113e538 cells/uL). Majority had CD4 > 200 cells/uL (64%), or were on highly active antiretroviral therapy (82%). Proportionately more males were observed in HIVpositive patients (91%), compared with controls (p < 0.05). Travel and pH1N1 exposure histories were not different between HIV-positive patients and controls. Interestingly, HIV-patients were more likely than controls to have received influenza vaccination within the past year (46% vs. 0% vs. 0%). Unsurprisingly, HIV-positive patients had a higher Charlson co-morbidity score than HIV-negative patients without co-morbidity (median 6 vs. 0, p Z 0.000), but did not have a significantly different score from HIV-negative patients with co-morbidities (p Z 0.175). Asthma (39%), chronic obstructive pulmonary disease (39%), and diabetes mellitus (21%) were most common co-morbidities in CG1. Among HIV-patients, 7 had AIDS; 3 had chronic liver disease, and one each with cardiovascular disease, cerebrovascular disease, dementia, and cancer. None had an active opportunistic infection at the time of pH1N1 infection. Presenting symptoms were similar between HIV-positive cases and controls (Table 2). Median illness duration at presentation was 1 day (range 0e6) for cases, 2 days (range 1e13) for CG1, and 2 days (range 0e9) for CG2. Fever (Case:91%, CG1:88%, CG2:97%) and cough (Case:91%, CG1:100%, CG2:88%) were the most common presenting symptoms. Similar findings were reported in immunosuppressed cancer patients.1 All HIV-positive and CG1 patients, and 97% of CG2 patients reported at least one respiratory symptom. HIV-positive cases were 5.3 times (95% CI 1.1e26.6) more likely than HIV-negative patients without any comorbidity to present with tachycardia (pulse rate >100
Letters to the Editor population of Afghan refugees in any single country, are residing in Pakistan.1 These refugees reside both in camps and urban slums, struggling against impoverishment, overcrowding, poor sanitation, lack of clean water, and of healthcare infrastructure.2,3 Human Immunodeficiency, Hepatitis B and C viruses (respectively, HIV, HCV, and HBV) share similar modes of transmission, that include blood to blood contact, sexual contact with infected person or vertical transmission (mother to child). Pakistan has an overall HIV prevalence of 0.1%, but within certain high risk groups, such as IDUs and MSM, concentrated HIV epidemics exist.4e6 According to a study which reviewed medical and public health literature regarding Hepatitis B and C in Pakistan, prevalence of 2.4 and 3%, respectively, were reported for the general population.7 Limited data exist on the prevalence of HIV, HCV and HBV in Afghanistan8e12 whereas no reports exist on the prevalence of these infections among Afghan refugees. As in other vulnerable populations, Injection drug users (IDUs), males who have sex with males (MSM), commercial sex workers, migrant workers and prisoners, are recognized as subgroups at high risk of the said infections among
*Corresponding author. Department of Infectious Diseases, Asan Medical Center, University of Ulsan College of Medicine, 86, Asanbyeongwon-gil, Songpa-gu, Seoul 138-736, Republic of Korea. Tel.: þ82 2 3010 3305; fax: þ82 3010 6970. E-mail address: [email protected] (S.-H. Kim) 31 August 2010 Available online 8 September 2010 ª 2010 The British Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jinf.2010.08.011
Concentrated epidemics of HIV, HCV, and HBV among Afghan refugees According to a 2007 United Nations High Commissioner for Refugees (UNHCR) report, 1.9 million, the largest
Table 1
Demographic details of study participants.
Categories
Total Z 556
HIV
HCV
Gender Males Females
410(73.7%) 146(26.2%)
33*(8.04%) 0*
167*(40.7%) 38*(26.0%)
40(9.75%) 11(7.53%)
Location Karachi Quetta
530(95.3%) 26(4.67%)
25*(4.71%) 8*(30.7%)
192(36.2%) 13(50.0%)
48(9.05%) 3(11.5%)
Marital Status Married Single Widow Unknown
443(79.6%) 107(19.2%) 1(0.17%) 5(0.89%)
27(6.09%) 6(5.60%)
169(38.1%) 35(32.7%) 1(100%)
45(10.1%) 6(5.60%)
Age Groups 10e19 years 20e29 years 30e39 years 40e49 years 50e59 years 60 and up Unknown
44(7.91%) 193(34.7%) 161(28.9%) 125(22.4%) 18(3.23%) 13(2.33%) 2(0.35%)
Profession Homemaker Driver Shop Keeper Student Guard Factory Hotel/Tea shop Other Labor/Loader/worker Unknown
69(12.4%) 50(8.99%) 91(16.3%) 38(6.83%) 35(6.29%) 29(5.21%) 21(3.77%) 80(14.3%) 70(12.5%) 73(13.1%)
0 0
0
HBV
0 0
3(6.81%) 14(7.25%) 11(6.83%) 5(4.00%)
9*(20.4%) 63(32.6%) 61(37.8%) 55(44.0%) 7(38.8%) 9*(69.2%) 1(50.0%)
3(6.81%) 14(7.25%) 12(7.45%) 18*(14.4%) 3(16.6%) 1(7.69%) 0
0* 6*(12.0%) 11*(12.0%) 2(5.26%) 1(2.85%) 0 4*(19.0%) 1(1.25%) 2(2.85%) 6(8.21%)
18*(26.0%) 20(40.0%) 37(40.6%) 7*(18.4%) 18(51.4%) 16(55.1%) 11(52.3%) 37(46.2%) 23(32.8%) 18(24.6%)
5(7.24%) 2(4.00%) 6(6.59%) 3(7.89%) 2(5.71%) 11*(37.9%) 1(4.76%) 7(8.75%) 6(8.57%) 8(10.9%)
0 0 0
The frequencies of all values are given in parentheses. *The association of demographics with HIV, HCV or HBV significant (p 0.05) calculated through Pearson Chi square test.
Letters to the Editor
435
the Afghan native12 and refugee populations.1,13,14 Following an analysis of HIV, HCV, and HBV among the Afghan refugees residing in Pakistan, we report here the existence of concentrated epidemics of all three infections in the refugee population. Samples were obtained through ‘Convenience Sampling’ of subjects attending antenatal clinics and persons participating in free health camps organized by the Infection Control Society, Pakistan, for screening of Hepatitis B, C and HIV, and for HBV vaccination. A total of 556 blood samples were collected from Afghan refugees. An informed consent was obtained from the study participants, and a questionnaire was administered to determine high risk behavior, prior to the collection of blood samples. The study was approved by the Ethical Review Committee, Aga Khan University, Karachi, Pakistan. Sera specimens were collected from the study subjects and Enzyme Linked Immuno Sorbent Assay (ELISA) was performed to check antibodies against HIV1/2 and HCV using Bioelisa HIV-1 þ 2 (rec) and Bioelisa HCV 4.0, respectively. Surface antigen against HBV was detected using Bioelisa HBsAg colour. For positive samples, results were confirmed twice using the same ELISA kits. Blood samples were collected from 556 participants. The majority of which came from various parts of Karachi (n Z 530) and a few from Quetta (n Z 26). The study group comprised mostly of males (73.7%) and most of the participants (34.7%) belonged to the age groups 20e29, representing a diversity of professions (Table 1). High risk behaviors such as drug use, injecting drugs and traveling abroad were observed in a considerable number of refugees (Tables 1 and 2). Out of 556 samples, 33 (5.93%) were found
Table 2
positive for anti-HIV antibodies, 205 (36.8%) for anti-HCV antibodies and 51 (9.17%) for Hepatitis B surface antigen. A total of 11 (1.97%) study subjects had HIV infection alone, 164 (29.4%) were infected only with HCV, whereas 30 (5.39%) were infected with HBV alone. 20 subjects (3.59%) were found to be co-infected with HCV and HIV, 19 (3.41%) had HCV and HBV, whereas 2 individuals (0.35%) carried all three viruses. Our study on the seroprevalence of HIV, HCV and HBV viruses among Afghan refugees in Pakistan revealed a higher occurrence of these viruses in the said group as compared to the general population of Pakistan. Risk factors possibly associated with these infections were drug abuse, transmigration, and, unsafe sexual behavior. A major high risk behavior observed among infected participants in this study was drug abuse (28.4%). Out of these drug users, some individuals reported the use of only injecting drugs (12.8%) while others stated to both smoking/inhaling as well as injecting drugs (18.5%). A significant correlation was observed between drug use and HIV infection in our study subjects (Table 2). In Afghanistan, opium and heroin have been used traditionally as medicine and for recreation. A study comparing the risk behaviors of Afghans and Pakistanis reports that Afghans are more likely than Pakistanis to have injected drugs, used opiate as their first illicit drug, report needle-sharing, or have a drug user in their family.15 Compared to the Pakistanis, Afghans have been reported to have lower awareness of HIV/AIDS.15 We observed a high prevalence of HIV (5.93%) in our study; very few participants, however, admitted to having multiple sex partners or contact with sex workers. In this group this may be
Correlation of viral infections with high risk behaviors.
Categories
Total Z 556
HIV
HCV
Drug Abuse Total Drug Abuse Only Smoked/Inhaled drugs Only Injected drugs Smoked/Inhaled þ Injected drugs
130(23.3%) 88(15.8%) 20(3.59%) 22(3.95%)
14*(10.7%) 6(6.81%) 2(10.0%) 6*(27.2%)
59*(45.3%) 40(45.4%) 7(35.0%) 12(54.5%)
Sexual History Homosexuality Multiple sex partners Travel History Total Travel History Abroad Afghanistan Saudi Arabia Sudan U.A.E. Afghanistan þ India Afghanistan þ Iran Afghanistan þ Saudi Arabia Afghanistan þ South Africa Afghanistan þ U.A.E. Others
6(1.07%) 2(0.35%) 260(46.7%) 214(38.4%) 6(1.07%) 1(0.17%) 17(3.05%) 1(0.17%) 1(0.17%) 3(0.53%) 5(0.89%) 6(1.07%) 6(1.07%)
0 2*(100%) 12(4.61%) 9(4.20%) 0 0 1(5.88%) 0 1*(100%) 0 1(20.0%) 0 0
3(50.0%) 2(100%) 78*(30.0%) 53*(24.7%) 4(66.6%) 1(100%) 10(58.8%) 1(100%) 1(100%) 1(33.3%) 4*(80.0%) 2(33.3%) 1(16.6%)
HBV 9(6.9%) 6(6.81%) 2(10.0%) 1(4.54%) 0 0 15*(5.76%) 11*(5.14%) 0 0 4*(23.5%) 0 0 0 0 0 0
The frequencies of all values are given in parentheses. *The association of high risk behavior with HIV, HCV or HBV significant (p 0.05) calculated through Pearson Chi square test.
436 attributed to social taboos regarding sexual matters.16 Frequent travel is also regarded as high risk behavior toward the spread of viral and other infections.14,17,18 Of those individuals who were infected in our study group, 27.2% travelled to Afghanistan (some made multiple visits), 5.69% visited the UAE and 1.62% went to Saudi Arabia. Statistical analysis revealed a strong correlation between travel to Afghanistan and infections with all three viruses (Table 2). Previously we have reported that Pakistanis who had travelled abroad and overseas contract workers, especially in the UAE countries, were potential source of concentrated HIV epidemics in Pakistan.19 This highlights a need for focused immigration policies that incorporate prevention and awareness programs for sexually-transmitted and blood-borne infections among refugees, migrant workers and travelers. In addition to single infections, we also observed coinfections in our study. Dually infected HIV patients are known to have unfavorable prognosis, both in the case of HIVeHCV20 as well as HIVeHBV21,22 combinations. While such individuals will need specially tailored treatment and management protocols, particular attention must be paid to timely diagnosis and to the control of high risk behaviors which can prevent the occurrence of multiple infections in the first place. Harm reduction programs for high risk groups are in place in Afghanistan23 as well as in Pakistan.24,25 The elevated incidence of viral infections in the Afghan refugee population reported here, however, highlights the need for the implementation of such programs especially targeted toward control and prevention of sexually-transmitted and blood-borne infections in this particular high group.
Funding support This study was partly funded by the Higher Education Commission, Pakistan, grant 20-775, and Pakistan Science Foundation, Pakistan, grant 232.
Conflict of interest None.
References 1. Rajabali A, Moin O, Ansari AS, Khanani MR, Ali SH. Communicable disease among displaced Afghans: refuge without shelter. Nat Rev Microbiol 2009;7(8):609e14. 2. Connolly MA, Gayer M, Ryan MJ, Salama P, Spiegel P, Heymann DL. Communicable diseases in complex emergencies: impact and challenges. Lancet 2004;364(9449): 1974e83. 3. Beckwith CG, DeLong AK, Desjardins SF, Gillani F, Bazerman L, Mitty JA, et al. HIV infection in refugees: a case-control analysis of refugees in Rhode Island. Int J Infect Dis 2009;13 (2):186e92. 4. Surveillance Data. Sindh AIDS Control Program. In: Government of Sindh Pakistan, editor. 2004. 5. Shah SA, Altaf A, Mujeeb SA, Memon A. An outbreak of HIV infection among injection drug users in a small town in Pakistan: potential for national implications. Int J STD AIDS 2004;15(3): 209.
Letters to the Editor 6. WHO/UNAIDS/UNICEF. Epidemiological Fact Sheet on HIV and AIDS Core data on epidemiology and response Pakistan. 2008; Update. 7. Ali SA, Donahue RM, Qureshi H, Vermund SH. Hepatitis B and hepatitis C in Pakistan: prevalence and risk factors. Int J Infect Dis 2009;13(1):9e19. 8. Todd CS, Abed AM, Strathdee SA, Scott PT, Botros BA, Safi N, et al. HIV, hepatitis C, and hepatitis B infections and associated risk behavior in injection drug users, Kabul, Afghanistan. Emerg Infect Dis 2007;13(9):1327e31. 9. Todd CS, Nasir A, Stanekzai MR, Bautista CT, Botros BA, Scott PT, et al. HIV, hepatitis B, and hepatitis C prevalence and associated risk behaviors among female sex workers in three Afghan cities. AIDS 2010;24(Suppl. 2):S69e75. 10. Todd CS, Ahmadzai M, Atiqzai F, Smith JM, Miller S, Azfar P, et al. Prevalence and correlates of HIV, syphilis, and hepatitis knowledge among intrapartum patients and health care providers in Kabul, Afghanistan. AIDS Care 2009;21(1): 109e17. 11. Todd CS, Ahmadzai M, Atiqzai F, Miller S, Smith JM, Ghazanfar SA, et al. Seroprevalence and correlates of HIV, syphilis, and hepatitis B and C virus among intrapartum patients in Kabul, Afghanistan. BMC Infect Dis 2008; 8:119. 12. UNGASS country progress report Afghanistan National AIDS Control Program, http://data.unaids.org/pub/Report/2010/afghanistan_ 2010_country_progress_report_en.pdf; August 30 2010. 13. Adoga MP, Banwat EB, Forbi JC, Nimzing L, Pam CR, Gyar SD, et al. Human immunonodeficiency virus, hepatitis B virus and hepatitis C virus: sero-prevalence, co-infection and risk factors among prison inmates in Nasarawa State, Nigeria. J Infect Dev Ctries 2009;3(7):539e47. 14. Khan S, Rai MA, Khanani MR, Khan MN, Ali SH. HIV-1 subtype A infection in a community of intravenous drug users in Pakistan. BMC Infect Dis 2006;6:164. 15. Zafar T, Brahmbhatt H, Imam G, ul Hassan S, Strathdee SA. HIV knowledge and risk behaviors among Pakistani and Afghani drug users in Quetta, Pakistan. J Acquir Immune Defic Syndr 2003;32(4):394e8. 16. Shafiq M, Ali SH. Sexually transmitted infections in Pakistan. Lancet Infect Dis 2006;6(6):321e2. 17. Resurgence of wild poliovirus type 1 transmission and consequences of importatione21 countries, 2002e2005. MMWR Morb Mortal Wkly Rep 2006;55(6):145e50. 18. Kazmi JH, Pandit K. Disease and dislocation: the impact of refugee movements on the geography of malaria in NWFP, Pakistan. Soc Sci Med 2001;52(7):1043e55. 19. Baqi S, Kayani N, Khan JA. Epidemiology and clinical profile of HIV/AIDS in Pakistan. Trop Doct 1999;29(3):144e8. 20. CDC. Hepatitis C virus and HIV coinfection. IDU HIV Prevention [cited; Available from: http://www.cdc.gov/IDU/hepatitis/ hepc_and_hiv_co.pdf; September 2002. 21. Dore GJ, Cooper DA. The impact of HIV therapy on co-infection with hepatitis B and hepatitis C viruses. Curr Opin Infect Dis 2001;14(6):749e55. 22. Soriano V on behalf of the SMART-INSIGHT study group. Antiretroviral therapy re-initiation and HBV rebound among HIV-HBV coinfected patients following ART interruption in the SMART Study. 16th Conference on Retroviruses and Opportunistic Infections, Montreal, February 2009. [Abstr. Q-111]. 23. Todd CS, Stibich MA, Stanekzai MR, Rasuli MZ, Bayan S, Wardak SR, et al. A qualitative assessment of injection drug use and harm reduction programmes in Kabul, Afghanistan: 2006e2007. Int J Drug Policy 2009;20(2):111e20. 24. Altaf A, Shah SA, Zaidi NA, Memon A, Nadeem ur R, Wray N. High risk behaviors of injection drug users registered with harm reduction programme in Karachi, Pakistan. Harm Reduct J 2007;4:7.
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25. Emmanuel F, Fatima M. Coverage to curb the emerging HIV epidemic among injecting drug users in Pakistan: delivering prevention services where most needed. Int J Drug Policy 2008;19 (Suppl. 1):S59e64.
Muhammad Rafiq Khanania Department of Microbiology, Dow University of Health Sciences, Karachi, Pakistan Amna S. Ansaria Saeed Khan Mehreen Somani Department of Biological and Biomedical Sciences, Aga Khan University, Karachi, Pakistan Shahana Urooj Kazmi Department of Microbiology, University of Karachi, Pakistan Syed H. Ali* Department of Biological and Biomedical Sciences, Aga Khan University, P.O. Box 3500, Karachi 74800, Pakistan Department of Microbiology, Dow University of Health Sciences, Karachi, Pakistan *Corresponding author. Tel.: +92 21 486 4433. E-mail address: [email protected] 30 August 2010 Available online 8 September 2010 ª 2010 The British Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jinf.2010.08.009
Pandemic (H1N1) 2009 influenza in HIV-infected adults: Clinical features, severity, and outcome
Dear Editor, We read with interest the paper by Redelman-Sidi et al. on 2009 H1N1 influenza infection in patients with cancer and hematopoietic stem cell transplant, reporting that these immunosuppressed patients did not have substantial risk for poor outcome from pH1N1.1 In April 2009, the World Health Organization was alerted of human infections with the novel pandemic (H1N1) 2009 (pH1N1) virus. The virus continues to spread globally.2 In Singapore, pH1N1 was first detected on May 26, 2009,3 in a returning student from New York. Rapid transmission occurred, despite containment measures.4,5 Although usually mild, pH1N1 can cause hospitalization in 2e5% of cases, and increase risk of complications in immunosuppressed persons.6e9 In HIV-positive individuals, a
MRK and ASA have equally contributed to this study.
pH1N1 fatalities have been reported.10e12 Although influenza has been described to cause significant morbidity and mortality among HIV-positive patients,13e18 the impact of pH1N1 on HIV-positive individuals is not well understood.10e12,19 To understand the epidemiological and clinical features, illness severity, and clinical outcomes of pH1N1 infection in HIV-positive adults, we conducted a matched case-control study at the Communicable Disease Centre at Tan Tock Seng Hospital Singapore, from July 1 to September 30, 2009. Case patients were HIV-positive adults who were confirmed with pH1N1 infection by polymerase chain reaction assay on respiratory specimens. Two control groups were randomly selected from adults confirmed with pH1N1 during the same period, but without a positive HIV status. Control group 1 (CG1) consisted of patients with at least one underlying medical condition other than HIV. Control group 2 (CG2) comprised those without any co-morbidity. Each HIV-patient was compared with 3 controls in each control group respectively, matched for age and hospitalization status (Table 1). Casenotes were reviewed for demographic and epidemiologic characteristics, pre-existing medical conditions, clinical signs and symptoms, haematological and biochemical markers, microbiological and radiological findings, treatment, and clinical outcomes. Eleven HIV-positive patients with pH1N1 were identified. Their median CD4 count was 223 cells/uL (range 113e538 cells/uL). Majority had CD4 > 200 cells/uL (64%), or were on highly active antiretroviral therapy (82%). Proportionately more males were observed in HIVpositive patients (91%), compared with controls (p < 0.05). Travel and pH1N1 exposure histories were not different between HIV-positive patients and controls. Interestingly, HIV-patients were more likely than controls to have received influenza vaccination within the past year (46% vs. 0% vs. 0%). Unsurprisingly, HIV-positive patients had a higher Charlson co-morbidity score than HIV-negative patients without co-morbidity (median 6 vs. 0, p Z 0.000), but did not have a significantly different score from HIV-negative patients with co-morbidities (p Z 0.175). Asthma (39%), chronic obstructive pulmonary disease (39%), and diabetes mellitus (21%) were most common co-morbidities in CG1. Among HIV-patients, 7 had AIDS; 3 had chronic liver disease, and one each with cardiovascular disease, cerebrovascular disease, dementia, and cancer. None had an active opportunistic infection at the time of pH1N1 infection. Presenting symptoms were similar between HIV-positive cases and controls (Table 2). Median illness duration at presentation was 1 day (range 0e6) for cases, 2 days (range 1e13) for CG1, and 2 days (range 0e9) for CG2. Fever (Case:91%, CG1:88%, CG2:97%) and cough (Case:91%, CG1:100%, CG2:88%) were the most common presenting symptoms. Similar findings were reported in immunosuppressed cancer patients.1 All HIV-positive and CG1 patients, and 97% of CG2 patients reported at least one respiratory symptom. HIV-positive cases were 5.3 times (95% CI 1.1e26.6) more likely than HIV-negative patients without any comorbidity to present with tachycardia (pulse rate >100