Urbanization of Yellow Fever Thomas P. Monath M.D. Risk of Urban Yellow fever • Vector – Ae. aegypti distribution, density – Vector competence • Virus – Proximity of and intensity of jungle cycle transmission • Human factors – Movements, migrations – Sanitation, crowding – Susceptibility • Immunization policy and vaccine coverage th th 18 -19 Centuries • Urban epidemics in US, Europe, West indies linked to colonial development and the slave trade • Most dreaded disease in North America – 500,000 cases, 100,000 deaths total – Texas to New England affected Historical YF Epidemics Massachusetts, 1801 Boston, Albany, 1734 1691, 1693, 1694, 1803, 1821 New Haven, 1747 New York, 1668, 1694, 1702, 1734, 1743, 1745, 1751, 1791, 1801, 1819, 1821, 1822, 1870 Alabama, 1821, 1854, 1873 PhiladelphiA 1668, 1693, 1694, 1699, 1751, 1778, 1791, 1793, 1802, 1803, 1805, 1819, 1820, 1821, 1867 Baltimore 1783, 1817, 1819, 1821 New Jersey, Washington, 1811 1825 Norfolk, VirginiA, 1801 1741, 1743 Mississippi, 1821, 1843, 1855, 1873, 1878 Memphis, 1828, 1873, 1879 Galveston, 1839, 1843, 1853, 1867, 1870 Vera Cruz, 1699, 1725 Mexico New orleans 1811, 1817, 1819, 1820, 1821, 822, 1824, 1827, 1828, 1829, 1837, 1841, 1847, 1854, 1856, 1867, 1873, 1878, 1905 Charleston, 1690, 1693, 1699, 1703, 1728, 1732, 1745, 1748, 1792, 1807, 1817, 1819, 1821, 1824, 1839, 1843, 1852, 1854, 1856, 1858, 1876 Mobile, 1825, 1827, 1829, 1837, 1839, 1843, 1847,1854, 1867 Florida, 1811, 1823, 1829, 1841, 1867 South carolina, 1877 © WHO 2005. 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Source: WHO Epidemic of 1878 • One of the worst disasters in US history • Mississippi Valley from New Orleans to Ohio • 20,000 deaths • Financial loss $200 million ($4.25 billion) • Disrupted commerce and society • Huge controversies over causality, transmission, value of quarantine Spanish American War, 1898 • Casualties – 260 die in battleship Maine explosion – 968 die in combat – 5000+ die of disease, mostly yellow fever Reed Commission- 1900 • Mosquito (Ae. aegypti) transmission (volunteer studies) • Incubation period 3-6 days • Extrinsic incubation period in mosquito required (12 days) • Filterable virus • Not transmissible by air, contact, fomites Conquest of Urban Yellow Fever William Crawford Gorgas 1854-1920 Control of Yellow Fever • Infected port cities (key centers) – Shipboard transmission • • • • • Low sanitation No piped water Water storage in and around homes High Ae. aegypti density and exposure Source reduction (larval breeding sites) eliminated risk of urban yellow fever Last Outbreak in United States 500 450 400 350 300 250 200 150 100 50 0 Water cisterns Ambulance 22 29 5 12 19 27 3 10 17 26 3 10 17 26 2 9 16 23 Jul Aug Sep Oct Nov New Orleans 1905 House screening gang (YF patients’ houses) Fumigation crew Jungle YF- 1937-1941 Alexander Haddow (1907-1976) Jorge Boshell Fred L Soper (1893-1977) Aedes aegypti eradication campaign in the Americas, initiated 1947 1940 1954 Trinidad, 1954 • 1907 Urban outbreak • 1914 Epizootic, few jungle cases • 1954 Epizootic-epidemic – Multiple isolations from Haemagogus – Island wide monkey deaths; 30% seropositive monkeys – 15 human cases, at least 3 Ae. aegypti-borne (1 from Port-ofSpain) – Human population not vaccinated – Ae. aegypti house indices >70% island-wide • First case diagnosed in April, next cases August – Ae. aegypti campaign initiated in June – Island wide immunization initiated July – Larger outbreak averted Distribution of Ae. aegypti in the Americas 1930's 1970 2007 Risk of urban YF Ae. aegypti Jungle YF 1998-2008 1998 Urban YF 2008 1 2 5 ≥10 Increase of Ae. aegypti Infestation by municipality, Brazil 1991-2000* 4000 3500 3000 2500 2000 1500 1000 500 0 1991 1992 Fonte:CR’s/SES’s FUNASA/CENEPI/GT-FAD 1993 1994 1995 1996 1997 1998 1999 2000 Yellow fever Vaccination • Population in endemic areas vaccinated – Mass campaigns – Routine EPI – High coverage in South America • Barrier to urbanization in Ae. aegypti infested towns in endemic region 19 30 19 34 19 38 19 42 19 46 19 50 19 54 19 58 19 62 19 66 19 70 19 74 19 78 19 82 19 86 19 90 19 94 19 98 Cases/deaths 200 120 100 80 40 Vaccinations 300 Cases, deaths, vaccinations BRAZIL 1930 - 2000 200 160 Risk of Urban Yellow Fever • Expansion of epizootic and jungle yellow fever to areas where vaccination coverage is low – Recent examples (Bolivia, Paraguay) • Movement of unvaccinated people from endemic to non-endemic zone Yellow fever Vaccination • Non-endemic areas – – – – Coastal zones, Altiplano, not vaccinated Large populations Receptive to YF introduction (Ae. aegypti present) High rate of migration, movement to/from endemic areas • Some countries extending vaccination to adjacent, within-border non-endemic areas – Bolivia, Peru • Vaccine shortages and YF vaccine related adverse events have limited policy implementation Brazil yellow fever endemic zone and population Urban Yellow Fever Santa Cruz, Bolivia 1998 • 6 cases (5 deaths) in city (pop 891,000) • 3 with no possible exposure to sylvatic transmission • Low immunization coverage ~41% • Other IgM + urban residents • High Ae aegypti Van der Stuyft et al., Lancet, 353:1558, 1999 Expansion of Epizootic YF 2008 To areas with low vaccination coverage First well documented urban outbreak in South America since 1942 (Asuncion) Paraguay, 2008 San Pedro Department First YF activity since 1974 SanEstanislao Estanislao San Firstcases casesdetected detected First Dec2007-Jan 2007-Jan2008 2008 Dec cases–likely likelyjungle jungleYF YF 88cases– Ringvaccination vaccination Ring Targetedvector vectorcontrol control Targeted SantaDomingo Domingo Santa February2008 2008 February cases(3 (3Female) Female) 77cases Ae.aegypti aegyptiand andSabethes Sabethes Ae. Sourceunclear unclear Source Ringvaccination vaccination Ring Vectorcontrol control Vector Caazaga Caazaga March2008 2008 March cases 44cases Junglevectors vectorsand andAe. Ae. Jungle aegyptipresent present aegypti SanLorenzo Lorenzo San February2008 2008 February cases(5 (5Female) Female) 99cases Ae.aegypti aegyptihouse houseindex index26% 26% Ae. Nojungle junglevectors vectors No Suburbanenvironment environment Suburban Massvaccination vaccination Mass Intensivevector vectorcontrol control Intensive Increasing risk of urban yellow fever in the American region VECTOR • Re-infestation of the South American continent by Ae. aegypti • Juxtaposition of urban and jungle cycles within endemic areas • Presence of vector in non-endemic (receptive) areas • High vector density in crowded, low socioeconomic areas of many cities • Insecticide resistance Increasing risk of urban yellow HUMAN HOST fever in the American region • Increased risk of introduction to receptive areas (unvaccinated, densely populated coastal zone) – Increased movement of migrant workers from nonendemic to endemic zones and back – Human urbanization, crowding, low socioeconomic and sanitary standards Major Urban Epidemic of Yellow Fever in South America • Not if • When? YF Epidemics, 1990-2008 2003, 2005 1986-94 1995, 2002 2000-01 1995, 1998 2001 1993, 1996 1992 1996 1990 1994 Aedes africanus Ae. luteocephalus Ae. furcifer Ae. vittatus Ae. opok Ae. metallicus Epidemic Vector 1986-94 1969 1965 1990 1978-79 1987 1940 1962-66 2001 1982-83 Ae. aegypti Ae. africanus Ae. luteocephalus Ae. simpsoni Ae. vittatus Ae. furcifer-taylori 1987-91 1970 1977 1970 1986 1983 1994 1993 1972 1992 AR=50.0/100,000 AR=2.7/100,000 AR=43.2/100,000 Breteau index (No. pos. containers/100 houses) and YF attack rate, the Gambia, 1978-79 Location Breteau (dry) Sambuldu 0 Attack rate Attack rate (rainy) (dry) 54.8 0 Serengaba 0 108.5 0 Sere N’Gai 1.5 34.3 0 Belai 9.5 19.7 6.6 Sare Bojo 9.6 8.5 12.8 Modi Jabbu 14.0 13.6 40.8 Germain et al Am J Trop Med Hyg 29:929, 1980 6000 5000 4000 3000 2000 1000 19 90 19 80 0 Ae. africanus Ae. aegypti • Ae. aegypti formosus – – – – Dark color Africa, sylvatic –tree-hold breeding Exophilic Zoophilic • Ae. aegypti aegypti – – – – Pale color Domestic breeding Endophilic Anthropophilic Trop Med Parasitol 1989;40:396 • Urban epidemic 1987, Nigeria – – – – Disease incidence high (2.9%) Breteau index very high (up to 676) Human biting rate high ( up to 3 mosq/man/hr) Ae. aegypti formusus Africa • Urban cycle has been a common event – Proximity of sylvatic and urban cycle – Depends on high vector density • Low vector competence – Urbanization of human population, increased communication, travel – Severe outbreaks in countries without immunization policy • Overall risk of urban yellow fever will be mitigated by – Mass immunization campaigns and routine immunization YF Vaccination in Africa 2000-2008 1990-99 No vaccination program Vaccination program 1980-89 1970-79 1960-69 0 20 40 60 80 100 Percent of endemic countries Source: WHO, 2008 Map showing countries with yellow fever vaccine in EPI with coverage attained by December 2007 YFV coverage >80% YFV coverage 50-79% YFV coverage <50% Endemic, no EPI Yellow fever distribution (reported cases 1987-2006) 260 73 1 94 1892 21 450 409 2* 1 678 19,226 1178 389 130 628 870 17* 60* 714 176 529 638 Distribution of Ae. aegypti 827 169 37 10 64 Introduction and Spread of Ae. aegypti-borne Diseases • Dengue • Chikungunya • Ross River Other potential urban vectors • Ae. albopictus – Low vector competence for YF Imported Cases of Yellow Fever Date Age/sex Vaccination Residence Exposure Outcome Oct 1979 42M No France Senegal Died Oct 1979 25M No France Senegal Died Aug 1985 27F No Netherlands W. Africa Survived Oct 1988 37F Yes Spain W.Africa Survived Apr 1996 53M No Switzerland Brazil Died Aug 1996 42M No USA Brazil Died Aug 1999 40M No Germany Ivory Coast Died Sep 1999 48M No USA Venezuela Died Nov 2001 47F No Belgium Gambia Died Mar 2002 47M No USA Brazil Died Distant Introduction Scenario • Dramatic disease, cases will likely come to light early • Outbreak will likely be contained rapidly • Incidence: few to tens of cases • High level public concern, panic, high demand for vaccine • Ring vaccination, mass vaccination • Serious vaccine related adverse events • Impact on trade, travel, tourism • Likely vaccine shortage Yellow fever 17D vaccine manufacturers 1970 2008 USA (Connaught) USA (sanofi pasteur) England (Wellcome) France (sanofi pasteur) France (Aventis-Pasteur) China (NVSI) USSR (Inst Polio VE) Russia (Inst Polio VE) Senegal (Pasteur) Senegal (Pasteur) Brazil (BioManguinhos) Brazil (BioManguinhos) Germany (R. Koch) Switzerland (Berna/Crucell) Netherlands (Inst Trop Med) India (CRI) Australia (CSL) Nigeria (Yaba) South Africa (NIV) Colombia (INS) 60m doses (90m needed) China (NVSI) 15m dose shortage 2008 (PAHO)
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