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A10
PRELIMINARY OBSERVATION OF THE EPIDEMIOLOGY OF SEASONAL AND PANDEMIC INFLUENZA A (H1N1) IN SOUTH AFRICA, 2009

B. D. Schoub, M.D., D.Sc., F.R.C.Path.,72 B. N. Archer, B.Med., M.P.H.,73 C. Cohen, M.Sc., M.B.B.Ch., F.C.Path.,73 D. Naidoo, M.Sc.,74 J. Thomas, M.B.B.Ch., F.C.Path.,74 C. Makunga, B.Sc.Hons., M.B.B.Ch.,74 M. Venter, Ph.D.,74 G. Timothy, M.B.B.Ch.,75 A. Puren, Ph.D., M.B.B.Ch.,73 J. McAnerney, R.N.,74 A. Cengimbo, M.B.B.Ch.,74 and L. Blumberg, M.B.B.Ch., M.Med.73

Introduction

The 2009-H1N1 influenza A pandemic took many by surprise. Unexpectedly arising in North America and spreading rapidly throughout the northern hemisphere summer, it encircled the globe within a couple of months. This event has again highlighted the crucial need for a more comprehensive global surveillance system for influenza (Lipsitch et al., 2009; Ortiz et al., 2009).

The World Health Organization (WHO) Influenza Programme has provided valuable information on circulating influenza viruses globally through its network of 128 national influenza centers in 99 countries, supported by five WHO collaborative centers (WHO, 2002, 2008, 2009a). Virus isolates from the majority of these laboratories provide the basis for the annual recommendation by WHO of the strains to be incorporated into the influenza vaccines for the Northern and Southern Hemispheres in February and September, respectively, of each year (WHO, 2009b,c).

However, the African continent is poorly capacitated for influenza surveillance (Schoub et al., 2002). Of the 46 countries constituting the WHO AFRO region, only 18 possess national influenza centers and only 10 are able to perform diagnostic PCR (WHO, 2009d,e). As of September 30, 2009, 12,382 cases of 2009-H1N1 influenza A were reported from this region; the great majority (93 percent) were reported from South Africa (WHO, 2009f).

Influenza Surveillance in South Africa

Systematic surveillance for influenza in South Africa dates back to 1984, when the first surveillance network of sentinel medical practitioners, the “Viral

72

National Institute for Communicable Diseases and University of the Witwatersrand, South Africa.

73

National Institute for Communicable Diseases, South Africa.

74

National Institute for Communicable Diseases and University of Pretoria, South Africa.

75

School of Public Health, University of the Witwatersrand, South Africa.



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283 APPENDIX A A10 PRELIMINARY OBSERVATION OF THE EPIDEMIOLOGY OF SEASONAL AND PANDEMIC INFLUENZA A (H1N1) IN SOUTH AFRICA, 2009 B. D. Schoub, M.D., D.Sc., F.R.C.Path.,72 B. N. Archer, B.Med., M.P.H.,73 C. Cohen, M.Sc., M.B.B.Ch., F.C.Path.,73 D. Naidoo, M.Sc.,74 J. Thomas, M.B.B.Ch., F.C.Path.,74 C. Makunga, B.Sc.Hons., M.B.B.Ch.,74 M. Venter, Ph.D.,74 G. Timothy, M.B.B.Ch.,75 A. Puren, Ph.D., M.B.B.Ch.,73 J. McAnerney, R.N.,74 A. Cengimbo, M.B.B.Ch.,74 and L. Blumberg, M.B.B.Ch., M.Med.73 Introduction The 2009-H1N1 influenza A pandemic took many by surprise. Unexpectedly arising in North America and spreading rapidly throughout the northern hemi- sphere summer, it encircled the globe within a couple of months. This event has again highlighted the crucial need for a more comprehensive global surveillance system for influenza (Lipsitch et al., 2009; Ortiz et al., 2009). The World Health Organization (WHO) Influenza Programme has provided valuable information on circulating influenza viruses globally through its network of 128 national influenza centers in 99 countries, supported by five WHO col- laborative centers (WHO, 2002, 2008, 2009a). Virus isolates from the majority of these laboratories provide the basis for the annual recommendation by WHO of the strains to be incorporated into the influenza vaccines for the Northern and Southern Hemispheres in February and September, respectively, of each year (WHO, 2009b,c). However, the African continent is poorly capacitated for influenza surveil- lance (Schoub et al., 2002). Of the 46 countries constituting the WHO AFRO region, only 18 possess national influenza centers and only 10 are able to per- form diagnostic PCR (WHO, 2009d,e). As of September 30, 2009, 12,382 cases of 2009-H1N1 influenza A were reported from this region; the great majority (93 percent) were reported from South Africa (WHO, 2009f). Influenza Surveillance in South Africa Systematic surveillance for influenza in South Africa dates back to 1984, when the first surveillance network of sentinel medical practitioners, the “Viral 72National Institute for Communicable Diseases and University of the Witwatersrand, South Africa. 73 National Institute for Communicable Diseases, South Africa. 74 National Institute for Communicable Diseases and University of Pretoria, South Africa. 75 School of Public Health, University of the Witwatersrand, South Africa.

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284 IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC Watch,” was established in Johannesburg (Besselaar et al., 2001; McAnerney et al., 1994; Schoub et al., 1986, 1994). Currently, the Viral Watch network consists of 243 sentinel sites, which provide clinical and epidemiological data on influenza in the community, as well as material for isolation and antigenic and molecular characterization of viruses, for input to WHO for decision making as to annual vaccine composition recommendations. In response to the 2009-H1N1 influenza A pandemic, the Viral Watch program was supplemented with an additional 10 hospital-based sites situated in all 9 provinces. Additional surveillance was provided by a Severe Acute Respiratory Infection (SARI) surveillance program, also established in 2009 in four large hospitals in three provinces. In addition, a large number of diagnostic specimens were received by the laboratory following widespread concern around the pandemic. Finally, active surveillance was intro- duced to collect information on all laboratory-confirmed cases due to 2009-H1N1 influenza A nationally, from both private and public laboratories. Up until 2009, the pattern of influenza isolations, as identified through the Viral Watch program, universally showed a typical unimodal distribution, as shown in Figure A10-1, with a median onset at week 23 (range 15-28), a median peak at week 27 (range 20-32) and a median duration of 10 weeks (range 7-17) (Figure A10-2). This pattern is consistent with other temperate Southern Hemi- sphere countries. The distribution of influenza subtypes is shown in Figure A10-3. Over the past 25 years, H3N2 was the dominant subtype in 13 of the years, H1N1 in 7, and influenza B in 2 of the years, with an equal distribution of all three in 2 years and an equal combination of H3N2 and B in one of the years. The 2009-H1N1 Influenza A Pandemic in South Africa The epidemic curve of the 2009-H1N1 influenza A pandemic as determined through active surveillance for all laboratory-confirmed cases nationally in South Africa, as of September 29th, is shown in Figure A10-4. The first case of 2009- H1N1 influenza A was confirmed in South Africa on June 13, some 2 months after that of the United States and a month or more after other Southern Hemisphere countries (Table A10-1). The reason for this inordinate delay in importation into South Africa is probably related to the relatively low volume of air traffic between it and North America (Chen and Wilson, 2008; Khan et al., 2009). The first confirmed South African case was in a healthy 16-year-old boy who had visited family in Texas and returned to South Africa on June 10th presenting with clinical signs and symptoms of influenza-like-illness (ILI). A positive diag- nosis of 2009-H1N1 influenza A infection was made at the National Institute for Communicable Diseases (NICD) using the CDC real-time (RT-) PCR protocol for the detection and characterization of swine influenza. He was treated with oseltamivir on day 3 after onset of symptoms and made an uneventful recovery; no secondary contacts were identified. During the following 2 weeks, NICD contin- ued to detect sporadic (H1N1) among individuals returning from North America,

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2005 2006 120 70 120 70 60 60 100 100 50 50 80 80 40 40 60 60 30 30 40 Isolation rate (%) 40 Isolation rate (%) 20 Number of isolates Number of isolates 20 20 20 10 10 0 0 0 0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 48 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 48 Week Week A H1N1 A H3N2 B Isolation rate A H1N1 A H3N2 B Isolation rate 2008 2007 75 140 70 40 120 60 30 100 50 50 80 40 20 60 30 25 40 **Isolation rate (%) Number of isolates Number of isolates Number Specimens 20 10 20 10 0 0 0 0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 Week Week A H1N1 A H3N2 B Isolation rate A H1N1 A H3N2 Influenza B Specimens 285 FIGURE A10-1 Influenza results by type and subtype: South Africa 2005-2008.

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R01627 vector editable landscape above, scaled for portrait below 286 IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC 2007 2006 • Median onset: 2005 2004 – Week 23 2003 2002 2001 – Range 15-28 2000 1999 • Median peak: 1998 1997 1996 – Week 27 1995 1994 – Range 20-32 1993 1992 • Median 1991 1990 1989 duration: 1988 1987 – 10 weeks 1986 1985 – Range 7-17 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 Apr May Jun Jul Aug Sep Epidemiological week Mean onset FIGURE A10-2 Onset and duration of influenza season, South Africa, 1985-2007. 100 80 60 Percentage 40 20 0 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 2005 2007 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 B A H3N2 A H1N1 FIGURE A10-3 Influenza strains detected, South Africa, 1984-2008. Figure A10-3

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287 APPENDIX A 2,500 25 Confirmed deaths Confirmed cases Number of Deaths Number of Cases 2,000 20 1,500 15 1,000 10 500 5 0 0 May 25-31 Jun 08-14 Jun 22-28 Jul 06-12 Jul 20-26 Aug 03-09 Aug 17-23 Aug 31-Sep 06 Sep 14-20 Sep 28-Oct 04 Oct 12-18 Oct 26-Nov 01 Nov 09-15 Nov 23-29 Dec 07-13 Week FIGURE A10-4 Epidemic curve of laboratory-confirmed pandemic 2009-H1N1 influenza A cases and deaths by week, South Africa, as of December 15, 2009 (n[cases] = 12,683). Figure A10-4 R01627 TABLE A10-1 Firstuneditable bitmapped image Confirmed Cases of 2009-H1N1 Influenza A type replaced Argentina May 16 Australia May 7 Chile May 17 New Zealand April 28 Uruguay May 27 USA April 17 South Africa June 13 South America, and Europe, with documented cases of local transmission resulting to a close household contact. A week later, on June 27th, an outbreak of H1N1 occurred at a sports event in Johannesburg, where 20 young athletes with ILI were confirmed at NICD as pandemic H1N1. The index case of this cluster was proba- bly an 18-year-old male attending from Zimbabwe, believed to have been infected while in transit (possibly through contact with other travellers). Over the next 2 weeks the number of confirmed cases rose steeply and, on July 13th, a month after the first case was diagnosed, over 100 cases had been confirmed in South Africa. At that stage the majority of cases were identified in the Gauteng province, the province with the largest population (incorporating both Johannesburg and Pretoria) and with the highest international exposure through OR Tambo Interna- tional Airport in Johannesburg. In conformance with the WHO recommendations

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288 IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC to cease universal laboratory testing of all suspected cases once the 100-case mark had been reached, the NICD and other academic centers reverted to testing only selected cases. Of the first 100 cases, 42 gave a travel history consistent with hav- ing acquired the infection abroad (Table A10-2). Epidemiological Characteristics As of September 29, 2009, a total of 11,729 cases had been confirmed nationally (Figure A10-4). The first death was confirmed on July 28th; a 22-year- old male student with no apparent comorbid condition. As of September 28th, 83 deaths had been laboratory-confirmed; the details are described below. The 2009 influenza season, as reflected through the Viral Watch program (community influenza surveillance), showed, for the first time, a bimodal curve (Figure A10-5). A similar bimodal distribution of 2009-H1N1 influenza A cases was also seen from the SARI program (Figure A10-6). Using mid-year population estimates (STATSSA, 2009), incidence data of laboratory-confirmed cases per 100,000 population were calculated for each of the nine provinces of South Africa (Table A10-3). The highest incidence was, not unexpectedly, seen in the Gauteng province, the commercial hub of the country, which is the smallest province geo- TABLE A10-2 Travel History of 42 Cases Within the First 100 Investigated North America 6 14% USA 6 South America 5 12% Argentina 2 Brazil 2 Chile 1 Europe 15 36% Other European Countries 5 Germany 1 Greece 1 Netherlands 1 Sweden 1 Turkey 1 UK 5 Asia 8 19% China 2 Singapore 4 Dubai 1 Bali 1 Other African Countries 3 7% Mauritius 2 Zimbabwe 1 Australia 5 12%

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289 APPENDIX A 300 80 250 60 % Detection rate 200 Number 150 40 100 20 50 0 0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 Week A awaiting typing Seasonal A (H1N1) A H3N2 B Pandemic A (H1N1) Detection rate FIGURE A10-5 Positive samples by influenza types and subtype: Viral Watch South Africa 2009. Figure A10-5 R01627 uneditable bitmapped image 50 50 45 45 40 40 35 35 Number of samples Detection rate (%) 30 30 25 25 20 20 15 15 10 10 5 5 0 0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 Weeks Detection rate A (Unsubtyped) A H1N1 (Seasonal) A H1N1 (Novel) A H3N2 B FIGURE A10-6 Severe acute respiratory illness (SARI) surveillance: respiratory virus Figure A10-6 report. R01627 uneditable bitmapped image type replaced

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290 IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC TABLE A10-3 Laboratory-Confirmed Pandemic 2009-H1N1 Influenza A Cases by Province, South Africa, as of December 15, 2009 Laboratory-Confirmed Cases Incidence Rate Province Cumulative Total (per 100,000 population) Eastern Cape 682 10.26 Free State 314 10.82 Gauteng 5,579 52.98 KwaZulu-Natal 2,258 21.61 Limpopo 545 10.43 Mpumalanga 500 13.86 Northern Cape 134 11.68 North West 465 13.48 Western Cape 2,113 39.44 Unknown 42 — South Africa Total 12,632 25.61 graphically but has the largest population, the highest population density, and the greatest contact internationally. This was followed by Western Cape (including Cape Town) and KwaZulu-Natal (including Durban). These provinces are also more urbanized and individuals there would be more likely to seek care and diagnostic testing for influenza than persons in more rural provinces. The age distribution of cases showed a predominance in children and young adults as also seen in countries throughout the world (CDC, 2009; Gilsdorf and Poggensee, 2009; Levy-Bruhl and Vaux, 2009; Lytras et al., 2009; Munayco et al., 2009; WHO, 2009g)—Figure A10-7, Table A10-4. The ages ranged from newborn to 90 years with a median age of 16 years. The age distribution curves for the different influenza subtypes as they presented in the Viral Watch program were compared. The pandemic 2009-H1N1 influenza A pattern was distinct from both the H3N2 of 2009 and the seasonal H1N1 of 2008 (Figures A10-8 and A10-9) and more closely resembled that of influenza B in 2009 (Figure A10-10). Preliminary Investigation of the First 100 Cases A more detailed follow-up investigation was carried out on the first 100 cases in South Africa. These cases, however, represented a more affluent, upper socio- economic section of the population and were also not representative of the racial composition of the South African population (Table A10-5). International travel within 7 days of onset of symptoms was reported in 42 cases and no travel or any contact with international travelers in the remainder. Only a minority of cases had recognized comorbid conditions—asthma (7), heart disease (5), preg-

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291 APPENDIX A 3000 2412 2500 2188 2082 Number of cases 2000 1500 1281 991 1000 775 597 558 450 500 359 316 238 130 58 62 0 <1 1-4 5-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65+ Age group (years) Figure A10-7 FIGURE A10-7 Number of laboratory confirmed pandemic 2009-H1N1 influenza A cases by age group, as of December 15, 2009 (n = 11,729). R01627 uneditable bitmapped image type replaced TABLE A10-4 Pandemic 2009-H1N1 Influenza A Cases by Age Group, South Africa, as of December 15, 2009 Incidence per 100,000a Age (years) Number Percentage of total 1-4 1,229 243 10 5-9 2,082 402 18 10-14 2,412 460 21 15-19 2,188 420 19 20-24 1,281 260 11 25-29 775 175 7 30-34 558 144 5 35-39 597 182 5 40-44 450 184 4 45-49 359 159 3 50-54 316 155 3 55-59 130 79 1 60-64 58 45 0.5 >65 62 26 0.5 aPopulation figures based on mid-year population estimates 2009 (STATSSA, 2009).

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292 IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC 50 40 30 Percentage 20 10 0 =60yr Age group A H3N2 Pandemic H1N1 FIGURE A10-8 Age distribution of patients with seasonal A H3N2 and pandemic 2009- H1N1 influenza A. 50 Figure A10-8 40 R01627 vector editable 30 Percentage 20 10 0 =60yr Age group Seasonal H1N1(2008) Pandemic H1N1 FIGURE A10-9 Age distribution of patients with seasonal A H1N1 (2008) and pandemic 2009-H1N1 influenza A. Figure A10-9 R01627 editable vectors

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293 APPENDIX A 50 40 30 Percentage 20 10 0 =60yr Age groups Infuenza B Pandemic H1N1 FIGURE A10-10 Age distribution of patients with influenza B and pandemic 2009-H1N1 influenza A. TABLE A10-5 Breakdown of First 100 Cases by Race Figure A10-10 Total South African Populationa H1N1 Cases R01627 Race N / Percentage N / Percentage editable vectors Asian 12 2.6 African 6 79.3 Mixed race 5 9.0 White 74 9.1 Unknown 3 — Total 100 100.0 aBased on 2009 mid-year population estimates (STATSSA, 2009). nancy (3), and obesity (2) (BMI > 30). The distribution of reported symptoms in these cases followed that seen generally throughout the world (Eurosurveillance, 2009b-e)—Figure A10-11. The mean time from onset of symptoms to presentation at a health facility was 2.0 days (SD 1.5 days, range 0-7 days) and symptom onset to recovery was 7.9 days (SD 1.5 days, range 0-7 days). Eleven cases were hospitalized, some as a precaution to isolate the patient and 6 developed complications including pneumonia (3), otitis media (1), myocarditis (1), and other (1).

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294 IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC 100 88 75 74 80 68 65 64 % of cases 55 60 47 40 32 25 18 20 13 7 0 Cough Sore throat Feeling feverish Nasal congestion Muscle pain Headache Fever >38 Sneezing Shortness of breath Diarrhea Vomiting Conjunctivitis Nausea FIGURE A10-11 Reported symptoms in first 100 confirmed cases, South Africa. Symptoms reported Preliminary Investigation of Deaths Figure A10-11 As of December 17, 2009, 92 laboratory-confirmed deaths were recorded R01627 in South Africa. The ages range from 3 days to 70 years, with a median age of 33 years—significantly higher than bitmapped image of 15 years. Deaths uneditable the overall median age were more common in females (60 percent) whereas the gender ratio was approx- type replaced imately equal in nonfatal cases. This was due, to a large extent, to the unusually large proportion of deaths in pregnant woman: 26 of the 91 cases (28 percent) with known clinical history. All but three of the deaths in pregnancy occurred in the third trimester (one in the second trimester and two in the puerperium). Of the 14 pregnancy-related fatal cases with known HIV status, 10 (71 percent) were HIV-positive; the national HIV seroprevalence in women attending public-sector antenatal clinics is 29 percent (Department of Health, 2009). Other comorbid con- ditions in this group were tuberculosis (TB) in 9 (11 percent) and pre eclampsia in 2 (8 percent). Of the 66 nonpregnant deaths, most (61 percent) were male. HIV was recorded in 6 of 17 patients (35 percent) as compared to the overall HIV preva- lence of 17 to 19 percent for South Africa (Department of Health, 2009). Active TB was found in 2 of 46 cases (4 percent) and other comorbid conditions included obesity (12 of 46; 26 percent), diabetes (11 of 45; 24 percent), and cardiac disease (8 of 44; 18 percent). Conclusion In many respects the 2009-H1N1 influenza A pandemic has behaved simi- larly to both developed and developing countries throughout the world. These

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295 APPENDIX A include age distribution, epidemiology, clinical features and overall relative mild- ness. The late introduction into South Africa appeared, to some extent, to be due to relatively lower air traffic levels and provided a window to observe any further genetic movement in the virus. Phenotypic changes in the virus were certainly not apparent from the clinical and epidemiological observations. Virological characterization is presently under way to determine antigenic drift, resistance, and presence of any virulence markers. Two particular risk groups in South Africa do perhaps need to be highlighted—those involving pregnancy and HIV. Although pregnancy is a well-recognized risk factor in H1N1 (Jamieson et al., 2009; Mangtani et al., 2009), South Africa experienced an unusually high number of women in late pregnancy who succumbed to H1N1. Second, the high rate of HIV positivity in both pregnant and nonpregnant individuals who died (consid- erably higher than the background HIV positivity in these two groups) needs special attention. In both groups the HIV prevalence was nearly double that of the respective national prevalence rates (Department of Health, 2009). These are, however, preliminary observations and are subject to potentially significant bias. For example, pregnancy may well be a factor that could increase the likelihood of a death being reported because of relatively greater access to a health facility. Also HIV may be artificially high as patients with more advanced disease and the stigma of HIV infection may be more likely to be treated and also more likely to succumb to H1N1. Whether persons living with HIV constitute a risk group for more severe influenza infection in the absence of secondary infection remains to be established (Kunisaki and Janoff, 2009). A study in an HIV-infected pediatric population in South Africa, also failed to demonstrate differences in outcome of influenza infection (Madhi et al., 2002). An understanding of these risk factors is of urgent importance, particularly in countries with a high prevalence of HIV and limited vaccine resources. References Besselaar, T. G., B. D. Schoub, and J. M. McAnerney. 2001. Phylogenetic studies of South African influenza A viruses: 1997-1999. In Options for the Control of Influenza IV, edited by A. D. M. E. Osterhaus, N. Cox, and A. W. Hampson. Proceedings of the Fourth International Conference on the Control of Influenza IV, Crete, Greece, September 23-28, 2000. Excerpta Medica 1219:139-145. CDC (Centers for Disease Control and Prevention). 2009. Update: Novel influenza A (H1N1) virus infections—worldwide, May 6, 2009. Morbidity and Mortality Weekly Report 58(RR17):453-457. Chen, L. H., and M. E. Wilson. 2008. The role of the traveler in emerging infections and magnitude of travel. Medical Clinics of North America 92(6):1409-1432. Department of Health. 2009. 2008 National Antenatal Sentinel HIV and Syphilis Prevalence Survey, South Africa. ECDC Working Group on Influenza A(H1N1)v. 2009. Preliminary analysis of influenza A(H1N1)v individual and aggregated case reports from EU and EFTA countries. Eurosurveillance 14(23), http://www.eurosurveillance.org/images/dynamic/EE/V14N23/art19238.pdf (accessed Octo- ber 22, 2009).

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