Trans R Soc Trop Med Hyg 2014; 108: 252–257 doi:10.1093/trstmh/tru043
REVIEW
Yellow fever, Asia and the East African slave trade John T. Catheya,* and John S. Marrb a
King Faisal Specialist Hospital and Research Centre, Riyadh, Saudi Arabia; bDepartment of Public Health Sciences, University of Virginia School of Medicine, Charlottesville, VA, USA *Corresponding author: Present address: PO Box 150, 414/18 Moo 12, Thappraya Road, Nongprue, Banglamung, Chon Buri, 20150 Thailand. Tel: +66 84 879 3208; E-mail: [email protected]
Yellow fever is endemic in parts of sub-Saharan Africa and South America, yet its principal vectors—species of mosquito of the genus Aedes—are found throughout tropical and subtropical latitudes. Phylogenetic analyses indicate that yellow fever originated in Africa and that its spread to the New World coincided with the slave trade, but why yellow fever has never appeared in Asia remains a mystery. None of several previously proposed explanations for its absence there is considered satisfactory. We contrast the trans-Atlantic slave trade, and trade across the Sahara and to the Arabian Peninsula and Mesopotamia, with that to Far East and Southeast Asian ports before abolition of the African slave trade, and before the scientific community understood the transmission vector of yellow fever and the viral life cycle, and the need for shipboard mosquito control. We propose that these differences in slave trading had a primary role in the avoidance of yellow fever transmission into Asia in the centuries before the 20th century. The relatively small volume of the Black African slave trade between Africa and East and Southeast Asia has heretofore been largely ignored. Although focal epidemics may have occurred, the volume was insufficient to reach the threshold for endemicity. Keywords: Aedes, Americas, Arbovirus, Asia, Flavivirus, Slave trade, Yellow fever
Introduction Yellow fever, an arthropod-borne hemorrhagic viral fever, is now endemic only in parts of tropical South America and subSaharan Africa.1 A continuing mystery is the absence of yellow fever from Asia, Australia and the Pacific Ocean islands, as its principal mosquito vector (Aedes spp., principally A. aegypti) occurs throughout most of the tropical and subtropical latitudes.1–3 A 1998 WHO report noted that none of the postulated explanations is satisfactory and that absence of the disease from Asia remains unexplained.4
Previously postulated explanations Several hypotheses, standing alone or in combination, have been proposed for yellow fever’s absence from parts of the tropics.4,5 Among them is that cross-immunity might exist between yellow fever and diseases caused by other flaviviruses present in Asia, such as dengue fever and others, so that prior exposure to another flavivirus would provide immunity to yellow fever. Antigenic similarities with dengue fever virus, present throughout Asia, may provide immunity to yellow fever.5 This possibility was supported by the findings of studies in rhesus monkeys immune to dengue and Kyasanur forest disease.6 The immune monkeys displayed higher survival rates, lower viraemia levels and prolonged survival times
compared with non-immune controls after challenge with virulent South American and African strains of the yellow fever virus, but death was not prevented in all immune monkeys. Another study also indicated the existence of cross-protection between certain flaviviruses and virulent yellow fever strains in vervet and rhesus monkeys, suggesting the possibility of interference with transmission of yellow fever virus in Africa.7 Some strains of Aedes are less competent vectors of yellow fever. Differences between strains of Aedes in susceptibility to oral infection as a result of genetic variation have been shown experimentally (using methods to estimate the natural field populations).8,9 The investigators concluded, however, that these variations by themselves would be unlikely to explain the geography of yellow fever endemicity, as many other factors are involved. In fact, West African Aedes strains in one study had relatively low susceptibility.9 Numerical and analytical modelling in a recent study by Amaku and colleagues favours the cross-immunity hypothesis to explain the absence of yellow fever in Asia, but is unable to exclude others.10 After incorporation of a new ‘African’ hypothesis into the model, they proposed that the relatively low prevalence in Africa of the Asian tiger mosquito (A. albopictus), in competition with A. aegypti, might explain the coexistence of yellow and dengue fever on that continent. Gubler earlier suggested that the recent spread of A. albopictus, a comparatively incompetent yellow fever vector, might decrease
# The Author 2014. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please e-mail: [email protected].
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Received 27 September 2013; revised 12 February 2014; accepted 13 February 2014
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The slave trade Phylogenetic analysis strongly supports an origin for yellow fever virus in Africa within the past 1500 years, and spread to the Americas coincident with the European trans-Atlantic or ‘Middle Passage’ slave trade that began in the 16th century and continued well into the 19th century.3,23 More recent phylogenetic data have included new and previously unpublished information on strains circulating in East Africa,24 which have ‘re-emerged’ in the past decade.25 The yellow fever virus may have originated in East and Central Africa and spread to Western Africa. These data support the theory that yellow fever epidemics may have occurred in East Africa in the past. Mercantile trade between Africa and Asia has existed for millennia; slave trade has been documented since the 7th century, and probably occurred earlier. Yellow fever did not become endemic in the Caribbean until the middle of the 18th century after the establishment of sugar plantations, which required a large slave-labour population and large quantities of stored water, used for sugar processing and for drinking.18 In a 1968 review, Haddow declared: ‘Few epidemiologists nowadays would challenge the view that yellow fever and its classical urban vector, A. aegypti, were transported to America in the slave ships’.26 If a cargo of closely quartered humans incubating the virus (Figure 1), together with standing water favouring mosquito reproduction, created conditions that favoured the spread of yellow fever across a vast ocean and into a non-immune population, then the
Figure 1. Conditions on board the slave ship Brookes in the 18th century; the ship could stow 454 African slaves (Library of Congress, open access).
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the risk of major epidemics of dengue or yellow fever.11 In 1934, Dudley described an epidemic in Brazil that was reportedly spread by a relatively incompetent vector (A. scapcularis) rather than A. aegypti, and thus warned that even a less efficient vector might be or have been capable of introducing the disease into Asia.12 Another explanation is simply that the disease was never introduced, at least not in sustainable numbers, to achieve endemicity in Asia.4 Monath noted that shipping trade was probably insufficient in the 18th and 19th centuries to carry yellow fever from South America or Africa to Asian ports, especially across the vast Pacific Ocean, and that the threat ended after eradication of yellow fever in Panama, Central America, during construction of the Panama Canal between the Atlantic and Pacific Oceans, the elucidation of the transmission cycle and vector of the disease, and subsequent improved mosquito control measures.5 Along the east coast of Africa, yellow fever has not been present in modern times (most of the region is considered at low risk today),2,13 but conditions are conducive to its presence and it may have been present in previous centuries. In 1946, the Tanganyika Territory (present-day Tanzania) and Zanzibar were reported free of recent infections.14 Tanzania was classified as endemic in the past, on the basis of serosurveys conducted in the 1940s and the finding in the 1950s of unvaccinated seropositive children on Zanzibar without a history of travel inland (although seropositivity may have been the result of infection by other flaviviruses).13 Two decades ago, the first recorded yellow fever outbreak in Kenya occurred (northeast of Lake Victoria in west-central provinces). Endemicity in Kenya seems to have been expanding from previous boundaries,15,16 and travellers are nowadays at risk of yellow fever in certain parts of the country.17 McNeill suggests that slaves from non-endemic areas who were eventually embarked from the west coast of Africa were infected during their long passages through endemic areas and survived.18 Slaves destined for the east coast came from the interior, especially after the 18th century.18 Gubler furthered the idea of logistics having a role in the absence of yellow fever in Asia, citing a low level of commerce between Asia and other continents when large, historic yellow fever epidemics were occurring and sailing ships were still the primary means of ocean transport.3 Elaborating on that idea, and assuming that the yellow fever virus could have left the coast of east Africa at some point in centuries prior to about 1900, we suggest that vast differences in the routes and volume of the slave trade to Asia compared with that to America may have been at least one factor, if not a primary factor, in yellow fever having never being introduced into Asia in the centuries before scientific understanding of the disease, and the development of control measures. As Manning notes: ‘In China, the presence of a large agricultural population . . . meant there was no great shortage of servile labor, and little need for slaves’.19 The same was probably true for mainland and maritime Southeast Asia. Concern arose about the spread of yellow fever to Asia after the opening of the Panama Canal in 1914, although much more was then known about the disease, and about the effectiveness of mosquito control and other measures to reduce the risk of transmission.4,20,21 A mosquito vector was suggested as early as 1848 by Notts, the theory formally articulated by the Cuban physician Finlay in 1881, and proven in 1900 by the Yellow Fever Commission under Reed, who also determined that a ‘filterable agent’ was the cause.22
J. T. Cathey and J. S. Marr
absence of a similar trade from the eastern or Swahili coast of Africa to as far as East and Southeast Asia may explain why yellow fever has never been introduced into that part of the world.
Volume and nature of the West African slave trade to the Americas
Volume and routes of the East African slave trade The East African slave trade has been studied very little, and it is probably impossible to make accurate estimates of its volume. Extrapolating from indirect evidence (literary sources) rather than direct data, Collins estimates that the volume of trade was about the same as that across the Atlantic (12.5 million) but was built up over nearly twice the timespan, i.e. over the period AD 800–1900. Before the establishment of Islam in the 7th century, little or no source material exists.28 Beginning in the 9th century, Arab and Muslim writers left descriptions of the slave trade from Africa to the Middle East and North Africa. Estimates become more reliable after the 16th century, when Europeans entered the trade. From AD 1600 to 1900, Collins estimates the slave trade at about 5.5 million, half that of the trans-Atlantic trade.28 Estimates by Eltis and Richardson over a similar period are smaller, but proportionally the same by route (Figure 2).27 The direction of the trade from AD 800 to 1900 was trans-Saharan primarily (7.3 million), and across the Red Sea (2.4 million).27 The trans-Saharan trade route was particularly difficult. The ‘Moors’ and other Arabs controlled the slave trade and the destinations were North Africa, Arabia, Mesopotamia, Anatolia, Persia and India. Major slave markets in North Africa were in Marrakech, Algiers, Tunis and Cairo. The traveller Ibn Battutah, a near contemporary of Marco Polo, noted in writings of his travels in the mid-14th century that from (West Africa) ‘come excellent slave-girls, eunuchs, and fabrics dyed with saffron.’30 In Arabia, the markets were in Jeddah, Mecca, and Aden and through the straits of Hormuz into the Arabian/Persian gulf. The remaining 2.9 million Africans were moved from the interior of East Africa to the coast and across the Indian Ocean.27 The annual monsoon winds carried trading dhows northeast then
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Figure 2. Estimated volume and routes of the African slave trade after 1500 (reproduced from Atlas of the Transatlantic Slave Trade with permission of Yale University Press).27
south as far as the Malabar coast of India and Sri Lanka (formerly Ceylon). Before the 19th century, the numbers were comparatively small.19 Beginning in the 19th century, the trade centered primarily on the offshore island of Zanzibar, under the control of Omanis. A substantial number of slaves were shipped around the Cape of Good Hope to Brazil. Remnants of the trade along the Indian west coast are reflected by the existence of the Siddi people of Black African descent who today live along the coast north of Mumbai (formerly Bombay) in the states of Gujarat and Hyderabad in India and Makran and Karachi in Pakistan. Another remnant population are the Sri Lankan Kaffirs. The beginnings of the Arab slave trade coincided with the expansion of Islam in the first few centuries AD.19 The holding of other Muslims as slaves was forbidden, so to meet demand slaves were taken during wars of expansion or by trading.30 Slaves came not only from Africa but also from the edges of the Islamic world in every direction, including whites to the north; the Slavs (origin of the term slave) from Eastern Europe and Circassians from the Caucasus (Circassian females were prized for their beauty and sought after as concubines). But most came from sub-Saharan Africa and from along the eastern coast, the Bar-el-Zanj (coast of the blacks). Arab traders ventured to East and Southeast Asia with the spread of Islam to that region, during the Tang (618–907) to Ming (1368–1644) Chinese dynasties. The Chinese and other Asians also came to the East African coast themselves to trade. The Chinese were interested in ivory, rhinoceros horn, leopard skins and tortoise shells, but bought few slaves.28 During the 10th century, an Arab geographer (al-Masudi of Baghdad) wrote that the primary commodity of maritime traders from East Africa to India and China at the time was ivory.31 In the early 19th century, many slaves remained on Zanzibar or nearby islands to work on the increasing numbers of plantations established for growing cloves, coconuts and grain. The end of slave exportation from the eastern coast began with the signing of an abolitionist treaty between the sultan of Zanzibar and the British in 1822. The African diaspora was primarily to the Caribbean, the Americas, the Arabian peninsula and Europe.32 Few if any Afro-descendants are found in the Far East or in Southeast Asia. Today, black and mixed-black people number in the millions in the Americas, while in China, and probably other parts of East
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Eltis and colleagues estimated that about 12.5 million enslaved Africans were shipped from the west coast of Africa across the Atlantic to the Caribbean and later to North and South America. With an average of 304 slaves per ship and as many as 600 in one voyage, 10.7 million disembarked in more than 35 000 voyages.27 The Voyages database starts in 1501 and includes records of voyages until the trade was finally suppressed in the latter half of the 19th century. The data are derived mostly from direct records (ships’ logs archived in port cities of Europe, from Liverpool to Lisbon) and estimates of the total volume are thought to be accurate. For the British, French and Dutch trade and for trade from Spain and Portugal to Brazil after 1750, the authors believe the database accounts for nearly all slave-trading voyages. By 1647–8, the years generally accepted for the first outbreak of yellow fever in the Caribbean and Yucatan Peninsula of Mexico, just over 700 000 slaves had been disembarked in the Americas. By 1761, when the disease was first considered endemic in Havana, for example, almost 5 million Africans had been disembarked.
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Asia, only a few thousand live among a population of more than a billion. Unlike in the Americas or Arabia, China and other countries in the region had sufficient population to meet the needs for large-scale labour-intensive work.
Nature of slavery in the Indian Ocean World
The reason for the absence of a historical introduction of yellow fever into Asia is largely of theoretical or academic interest. Focal outbreaks of yellow fever may have occurred throughout the world in the past (as they may have in the Americas before the first outbreak in Barbados in 1647), but are not recorded.4,22 A search of Indian and Chinese medical history might reveal descriptions of haemorrhagic diseases in Asia that might have been yellow fever, but could also have been many other diseases (Weil’s disease, dengue haemorrhagic fever, Kyasanur forest disease, Crimean–Congo haemorrhagic fever virus or hantavirus variants).The slave trade hypothesis might be questioned by noting that a large number of potentially infected Indian troops left Africa en masse for Asia (the Indian subcontinent) in pre-vaccine days after World War I and endemicity did not follow, but that event hardly compared with the conditions of transportation and pattern of continual reintroduction during the decades-long slave trade to the Americas. The Indian troops were probably aware of the need for shipboard mosquito control. Indian expeditionary forces under British command fought mainly in East Africa,39 while the distribution of yellow fever at that time was largely confined to coastal West Africa.20 The Indian Ocean was the only potential route to Asia for yellow fever in the days before air travel. The arid environment of North Africa, the Arabian peninsula and Mesopotamia and lack of a suitable non-human primate reservoir would not support maintenance of a sylvatic or savannah cycle. These landmasses would have provided a buffer between Africa and suitable yellow fever environments farther to the southeast. But today the potential for direct introduction into tropical regions to the east, where there has been no previous exposure in the population, remains a major public health concern. The recent outbreak in Sudan is a reminder that yellow fever remains a threat nowadays and that outbreaks in East Africa are not uncommon.40 Since the development of a yellow fever vaccine early in the 20th century and institution of mosquito control measures, large-scale yellow fever epidemics are mostly a thing of the past. Smaller outbreaks still occur regularly and are increasing, particularly in Africa; this is in part because of the lack of vaccination in developing countries in endemic areas. Present-day air travel replicates and magnifies the conditions for spread of a virus across vast spaces. However, the size of the mosquito vector population transported via an aircraft and modern disinsection practices probably make this an unlikely, although not impossible, means of sparking an epidemic of yellow fever in a distant land.41 In 1934, Dudley raised the concern that yellow fever might at that time still spread from the eastern coast of Africa to Asia, expressing the possibility of ‘a holocaust to which all the historical epidemics would be as the Battle of Waterloo was to the Great War’.12 The requirement of a yellow fever vaccination certificate by Asian countries for people entering from yellow fever endemic areas provides little guarantee that yellow fever cannot still enter Asia. Shortages of yellow fever vaccine in India for a time presented a problem for individuals traveling to Africa, who are required to have a certificate on return. Fake vaccination certificates have been sold in Kenya42 and Nigeria43 in the past and more recently in India.44 It could be that all the proposed explanations for the lack of yellow fever transmission to Asia before modern understanding
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In one volume of a series of specialist studies on slavery in the Indian Ocean World (considered to range from China to Southeast and South Asia, the Middle East and Africa), Campbell makes it clear that ‘the essential features of the slave-trade and slavery in the Indian Ocean World contrast sharply with those of the trans-Atlantic slave-trade and plantation slavery in the Americas’.33 Most documentation suggests that slaves in Arabia served as domestics, performing menial tasks. Eunuchs were used to guard the harem or serve as custodians in mosques and other important places. However, the impression that most slaves were used primarily in those roles may only reflect the lack of documentation of practices in the countryside in the early years of Islam.30 There is evidence that slaves were used on date plantations, in the mines and in the draining of marshes, activities more on the scale of slavery in the Americas, which required a large manual workforce. Ibn Battutah described salt mining in the western Sahara by slaves owned by Berbers.34 In addition to mining salt in the Sahara, black slaves were used for gold mining in Nubia and the draining of marshes in the lower reaches of the Tigris–Euphrates river.27 One of the largest slave revolts in history occurred in the 9th century among Zanj slaves involved in draining the Mesopotamian marshes.31,35 The Zanj Rebellion, involving half a million African slaves, took place near Basra at the head of the Gulf and lasted for 15 years. Historian Andrew Watson hypothesised the existence of an Arab agricultural revolution in the ‘Fertile Crescent’, the area including the Nile River valley and fertile areas of the Shatt al-Arab around the Tigris–Euphrates river system from the 8th to the 13th century.36 The resulting plantation economy would have required large numbers of slaves to perform the fieldwork. Slaves who converted to Islam were later freed and assimilated into the population (in contrast to the Afro-American experience).30 A substantial portion of the population of countries on the Arabian Peninsula today are of black African or mixed descent. They are Muslim, Arab-speaking and many are in the professions and other positions of high socioeconomic status. In East and Southeast Asia in contrast, the nature of the work of black African slaves was much different. A colony of Arab traders resided in Guangzhou (formerly Canton) at the mouth of the Pearl River near present-day Hong Kong, but slaves were not a primary commodity.37 In Guangzhou, it was fashionable for a time among the wealthy to have blacks as ‘ornamentals’ so to speak— as doormen and guards, and also as concubines and for domestic work—not in the vast numbers for heavy labour as in the Americas and in the Middle East. Needham noted: ‘The Chinese and other Asian nations had been using negro slaves for many centuries, but the fact that their slavery was basically domestic kept the practice within bounds [short of the massive imports for plantation labor that dominated the Atlantic Trade]’.38 Chinese traders went to Africa and traded directly with Arab traders and Africans, but the purchase of slaves was not nearly on the scale as that of Arabs and Europeans.
Discussion
J. T. Cathey and J. S. Marr
of the disease are correct, but individually each was insufficient to account for the disease’s sustained absence from that continent. In epidemic modelling terms, even if the yellow fever virus reached the Asian Far East, the basic reproduction number never reached the threshold value to establish endemicity.45 In contrast, the continuous and voluminous African slave trade to the Americas was sufficient to cause focal epidemics and for yellow fever eventually to become endemic in regions of the tropical world that could sustain the transmission cycle.
Acknowledgements: We thank Drs Thomas Monath and Jack Woodall for critical reviews, Safiyya Mohamed Ali for editorial assistance and David Connell and Reina Tejano for assistance with the images.
14 Mahaffy A., Smithburn K, Hughes T. The distribution of immunity to yellow fever in central and East Africa. Trans R Soc Trop Med Hyg 1946;40:57–82. 15 Ellis BR, Sang RC, Horne KM et al. Yellow fever virus susceptibility of two mosquito vectors from Kenya, East Africa. Trans R Soc Trop Med Hyg 2012;106:387–9. 16 Sanders EJ, Marfin AA, Tukei PM et al. First recorded outbreak of yellow fever in Kenya, 1992–1993. I. Epidemiologic investigations. Am J Trop Med Hyg 1998;59:644–9. 17 Monath TP, Gershman M, Hill DR et al. Yellow fever recommendations for tourists to Kenya: a flawed risk assessment. J Trav Med 2009:16;146; author reply 146–7. 18 McNeill J. Mosquito Empires: Ecology and War in the Greater Caribbean, 1620–1914. Cambridge: Cambridge University Press; 2010. p. 390. 19 Manning P. Slavery and African Life: Occidental, Oriental, and African Slave Trades. Cambridge: Cambridge University Press; 1990. p. 52.
Funding: None.
20 Frierson JG. The yellow fever vaccine: A history. Yale J Biol Med 2010;83:77–85.
Competing interests: None declared.
21 Stitt ER. The Diagnostics and Treatment of Tropical Diseases, 3rd edn, revised. Miami: HardPress Publishing; 1919.
Ethical approval: Not required.
22 Carter HR. Yellow Fever: An epidemiological and historical study of its place of origin. Philadelphia, PA: Williams & Wilkins; 1931. p. 308.
References
23 Bryant JE, Holmes EC, Barrett ADT. Out of Africa: A molecular perspective on the introduction of yellow fever virus into the Americas. PLoS Pathog 2007;3:e75.
1 Monath TP. Yellow fever: an update. Lancet Infect Dis 2001;1:11–20. 2 Rogers DJ, Wilson AJ, Hay SI, Graham AJ. The global distribution of yellow fever and dengue. Adv Parasitol 2006;62:181–220. 3 Gubler DJ. The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comp Immunol Microbiol Infect Dis 2004;27:319–30. 4 Vainio J, Cutts F., Yellow Fever. WHO Division of Emerging and other Communicable Diseases Surveillance and Control. Geneva: WHO; 1998 [accessed 22 December 2012]. 5 Monath TP. The absence of yellow fever in Asia: hypotheses. A cause for concern? Virus Inf Exch Newslett 1989;106–7. 6 Theiler M, Anderson CR. The relative resistance of dengueimmune monkeys to yellow fever virus. Am J Trop Med and Hyg 1975;24:115–7. 7 Henderson BE, Cheshire PP, Kirya GB, Lule M. Immunologic studies with yellow fever and selected African Group B arboviruses in rhesus and vervet monkeys. Am J Trop Med Hyg 1970;19:110–8. 8 Wallis G, Aitken T, Beaty B et al. Selection for susceptibility and refractoriness of Aedes aegypti to oral infection with yellow fever virus. Am J Trop Med Hyg 1985;34:1225–31. 9 Tabachnick WJ, Wallis GP, Aitken TH et al. Oral infection of Aedes aegypti with yellow fever virus: geographic variation and genetic considerations. Am J Trop Med Hyg 1985;34:1219–24. 10 Amaku M, Coutinho FAB, Massad E. Why dengue and yellow fever coexist in some areas of the world and not in others? Biosystems 2011;106:111–20.
24 Beck A, Guzman H, Li L et al. Phylogeographic reconstruction of African yellow fever virus isolates indicates recent simultaneous dispersal into East and West Africa. PLoS Negl Trop Dis 2013;7: e1910. 25 Ellis BR, Barrett AD. The enigma of yellow fever in East Africa. Rev Med Virol 2008;18:331–46. 26 Haddow AJ. The natural history of yellow fever in Africa. Proc R Soc Edinb Section B. Biology 2012;70:191–227. 27 Eltis D, Richardson D. Atlas of the Transatlantic Slave Trade. New Haven, CT: Yale University Press; 2010. p. 336. 28 Collins RO. The African slave trade to Asia and the Indian Ocean Islands. Afr Asian Stud 2006;5:325–46. 29 Battuta I. The Travels of Ibn Battuta: In the Near East, Asia and Africa. New York: Cosimo; 2010. p. 270. 30 Lewis B. Race and Slavery in the Middle East: An Historical Enquiry. Oxford: Oxford University Press, USA; 1992. p. 224. 31 Oliver R, Fagan BM. Africa in the Iron Age: c.500 BC to AD 1400. New York: Press Syndicate of the University of Cambridge; 1975. p. 192. 32 Manning P. The African Diaspora: A history through culture (Columbia Studies in International and Global History). New York: Columbia University Press; 2009. 33 Campbell G, editor. Structure of Slavery in Indian Ocean Africa and Asia (Slave Societies). New York: Frank Cass Publishers; 2003. p. 256.
11 Gubler DJ. Aedes albopictus in Africa. Lancet Infect Dis 2003;3:751–2.
34 Battutah I. The Travels of Ibn Battutah. Mackintosh-Smith T, editor. London: Macmillan; 2003. p. 400.
12 Dudley SF. Can yellow fever spread into Asia? An essay on the ecology of mosquito-borne disease. J Trop Med Hyg 1934;37:273–8.
35 Furlonge ND. Revisiting the Zanj and Re-Visioning Revolt: Complexities of the Zanj Conflict (868–883 AD). Negro Hist Bull 1999;62:7.
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Authors’ contributions: JC conceived the idea of the review and wrote the manuscript; JM made critical suggestions and contributed to content and writing. Both authors read and approved the final manuscript. JC is guarantor of the paper.
13 Jentes ES, Poumerol G, Gershman MD et al. The revised global yellow fever risk map and recommendations for vaccination, 2010: consensus of the Informal WHO Working Group on Geographic Risk for Yellow Fever. Lancet Infect Dis 2011;11:622–32.
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36 Watson A. The Arab agricultural revolution and its diffusion, 700–1100. J Econ Hist 1974; 34:8–35. 37 Wilensky J. The Magical Kunlun and ‘Devil Slaves’: Chinese perceptions of dark-skinned people and Africa before 1500. In: Mair VH, editor. The Sino–Platonic Papers (online) Chapters 1 and 2. http://www. sino-platonic.org/complete/spp122_chinese_africa.pdf [accessed December 2012]. 38 Needham J. Science and Civilisation in China. Volume 4, Physics and Physical Technology: Part 3, Civil Engineering and Nautics. Cambridge: Cambridge University Press; 1971. p. 1171. 39 Riddick JF. The History of British India: A chronology. Westport, CT: Praeger; 2006. p. 384. 40 Markoff L. Yellow fever outbreak in Sudan. N Engl J Med 2013; 368:689–91.
41 Hardiman M, Wilder-Smith A. The revised international health regulations and their relevance to travel medicine. J Trav Med 2007;14:141–4. 42 Siringi S. Fake health certificate racket rife in Kenya. Lancet Infect Dis 2002;2:454. 43 ProMED-mail. Yellow Fever - Africa (22): Nigeria, fake cards. ProMED-mail 27 Aug 2013: 20130827.1906967. http://www. promedmail.org [accessed 19 September 2013]. 44 ProMED-mail. Yellow fever vaccine availability - India (04). ProMED-mail 20 July 2013: 20130720.1835444. http://www. promedmail.org [accessed 19 September 2013]. 45 Smith DL, Battle JE, Hay SI et al. Ross, MacDonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathogens 2012; 8:e1002588.
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257
REVIEW
Yellow fever, Asia and the East African slave trade John T. Catheya,* and John S. Marrb a
King Faisal Specialist Hospital and Research Centre, Riyadh, Saudi Arabia; bDepartment of Public Health Sciences, University of Virginia School of Medicine, Charlottesville, VA, USA *Corresponding author: Present address: PO Box 150, 414/18 Moo 12, Thappraya Road, Nongprue, Banglamung, Chon Buri, 20150 Thailand. Tel: +66 84 879 3208; E-mail: [email protected]
Yellow fever is endemic in parts of sub-Saharan Africa and South America, yet its principal vectors—species of mosquito of the genus Aedes—are found throughout tropical and subtropical latitudes. Phylogenetic analyses indicate that yellow fever originated in Africa and that its spread to the New World coincided with the slave trade, but why yellow fever has never appeared in Asia remains a mystery. None of several previously proposed explanations for its absence there is considered satisfactory. We contrast the trans-Atlantic slave trade, and trade across the Sahara and to the Arabian Peninsula and Mesopotamia, with that to Far East and Southeast Asian ports before abolition of the African slave trade, and before the scientific community understood the transmission vector of yellow fever and the viral life cycle, and the need for shipboard mosquito control. We propose that these differences in slave trading had a primary role in the avoidance of yellow fever transmission into Asia in the centuries before the 20th century. The relatively small volume of the Black African slave trade between Africa and East and Southeast Asia has heretofore been largely ignored. Although focal epidemics may have occurred, the volume was insufficient to reach the threshold for endemicity. Keywords: Aedes, Americas, Arbovirus, Asia, Flavivirus, Slave trade, Yellow fever
Introduction Yellow fever, an arthropod-borne hemorrhagic viral fever, is now endemic only in parts of tropical South America and subSaharan Africa.1 A continuing mystery is the absence of yellow fever from Asia, Australia and the Pacific Ocean islands, as its principal mosquito vector (Aedes spp., principally A. aegypti) occurs throughout most of the tropical and subtropical latitudes.1–3 A 1998 WHO report noted that none of the postulated explanations is satisfactory and that absence of the disease from Asia remains unexplained.4
Previously postulated explanations Several hypotheses, standing alone or in combination, have been proposed for yellow fever’s absence from parts of the tropics.4,5 Among them is that cross-immunity might exist between yellow fever and diseases caused by other flaviviruses present in Asia, such as dengue fever and others, so that prior exposure to another flavivirus would provide immunity to yellow fever. Antigenic similarities with dengue fever virus, present throughout Asia, may provide immunity to yellow fever.5 This possibility was supported by the findings of studies in rhesus monkeys immune to dengue and Kyasanur forest disease.6 The immune monkeys displayed higher survival rates, lower viraemia levels and prolonged survival times
compared with non-immune controls after challenge with virulent South American and African strains of the yellow fever virus, but death was not prevented in all immune monkeys. Another study also indicated the existence of cross-protection between certain flaviviruses and virulent yellow fever strains in vervet and rhesus monkeys, suggesting the possibility of interference with transmission of yellow fever virus in Africa.7 Some strains of Aedes are less competent vectors of yellow fever. Differences between strains of Aedes in susceptibility to oral infection as a result of genetic variation have been shown experimentally (using methods to estimate the natural field populations).8,9 The investigators concluded, however, that these variations by themselves would be unlikely to explain the geography of yellow fever endemicity, as many other factors are involved. In fact, West African Aedes strains in one study had relatively low susceptibility.9 Numerical and analytical modelling in a recent study by Amaku and colleagues favours the cross-immunity hypothesis to explain the absence of yellow fever in Asia, but is unable to exclude others.10 After incorporation of a new ‘African’ hypothesis into the model, they proposed that the relatively low prevalence in Africa of the Asian tiger mosquito (A. albopictus), in competition with A. aegypti, might explain the coexistence of yellow and dengue fever on that continent. Gubler earlier suggested that the recent spread of A. albopictus, a comparatively incompetent yellow fever vector, might decrease
# The Author 2014. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please e-mail: [email protected].
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Received 27 September 2013; revised 12 February 2014; accepted 13 February 2014
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The slave trade Phylogenetic analysis strongly supports an origin for yellow fever virus in Africa within the past 1500 years, and spread to the Americas coincident with the European trans-Atlantic or ‘Middle Passage’ slave trade that began in the 16th century and continued well into the 19th century.3,23 More recent phylogenetic data have included new and previously unpublished information on strains circulating in East Africa,24 which have ‘re-emerged’ in the past decade.25 The yellow fever virus may have originated in East and Central Africa and spread to Western Africa. These data support the theory that yellow fever epidemics may have occurred in East Africa in the past. Mercantile trade between Africa and Asia has existed for millennia; slave trade has been documented since the 7th century, and probably occurred earlier. Yellow fever did not become endemic in the Caribbean until the middle of the 18th century after the establishment of sugar plantations, which required a large slave-labour population and large quantities of stored water, used for sugar processing and for drinking.18 In a 1968 review, Haddow declared: ‘Few epidemiologists nowadays would challenge the view that yellow fever and its classical urban vector, A. aegypti, were transported to America in the slave ships’.26 If a cargo of closely quartered humans incubating the virus (Figure 1), together with standing water favouring mosquito reproduction, created conditions that favoured the spread of yellow fever across a vast ocean and into a non-immune population, then the
Figure 1. Conditions on board the slave ship Brookes in the 18th century; the ship could stow 454 African slaves (Library of Congress, open access).
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the risk of major epidemics of dengue or yellow fever.11 In 1934, Dudley described an epidemic in Brazil that was reportedly spread by a relatively incompetent vector (A. scapcularis) rather than A. aegypti, and thus warned that even a less efficient vector might be or have been capable of introducing the disease into Asia.12 Another explanation is simply that the disease was never introduced, at least not in sustainable numbers, to achieve endemicity in Asia.4 Monath noted that shipping trade was probably insufficient in the 18th and 19th centuries to carry yellow fever from South America or Africa to Asian ports, especially across the vast Pacific Ocean, and that the threat ended after eradication of yellow fever in Panama, Central America, during construction of the Panama Canal between the Atlantic and Pacific Oceans, the elucidation of the transmission cycle and vector of the disease, and subsequent improved mosquito control measures.5 Along the east coast of Africa, yellow fever has not been present in modern times (most of the region is considered at low risk today),2,13 but conditions are conducive to its presence and it may have been present in previous centuries. In 1946, the Tanganyika Territory (present-day Tanzania) and Zanzibar were reported free of recent infections.14 Tanzania was classified as endemic in the past, on the basis of serosurveys conducted in the 1940s and the finding in the 1950s of unvaccinated seropositive children on Zanzibar without a history of travel inland (although seropositivity may have been the result of infection by other flaviviruses).13 Two decades ago, the first recorded yellow fever outbreak in Kenya occurred (northeast of Lake Victoria in west-central provinces). Endemicity in Kenya seems to have been expanding from previous boundaries,15,16 and travellers are nowadays at risk of yellow fever in certain parts of the country.17 McNeill suggests that slaves from non-endemic areas who were eventually embarked from the west coast of Africa were infected during their long passages through endemic areas and survived.18 Slaves destined for the east coast came from the interior, especially after the 18th century.18 Gubler furthered the idea of logistics having a role in the absence of yellow fever in Asia, citing a low level of commerce between Asia and other continents when large, historic yellow fever epidemics were occurring and sailing ships were still the primary means of ocean transport.3 Elaborating on that idea, and assuming that the yellow fever virus could have left the coast of east Africa at some point in centuries prior to about 1900, we suggest that vast differences in the routes and volume of the slave trade to Asia compared with that to America may have been at least one factor, if not a primary factor, in yellow fever having never being introduced into Asia in the centuries before scientific understanding of the disease, and the development of control measures. As Manning notes: ‘In China, the presence of a large agricultural population . . . meant there was no great shortage of servile labor, and little need for slaves’.19 The same was probably true for mainland and maritime Southeast Asia. Concern arose about the spread of yellow fever to Asia after the opening of the Panama Canal in 1914, although much more was then known about the disease, and about the effectiveness of mosquito control and other measures to reduce the risk of transmission.4,20,21 A mosquito vector was suggested as early as 1848 by Notts, the theory formally articulated by the Cuban physician Finlay in 1881, and proven in 1900 by the Yellow Fever Commission under Reed, who also determined that a ‘filterable agent’ was the cause.22
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absence of a similar trade from the eastern or Swahili coast of Africa to as far as East and Southeast Asia may explain why yellow fever has never been introduced into that part of the world.
Volume and nature of the West African slave trade to the Americas
Volume and routes of the East African slave trade The East African slave trade has been studied very little, and it is probably impossible to make accurate estimates of its volume. Extrapolating from indirect evidence (literary sources) rather than direct data, Collins estimates that the volume of trade was about the same as that across the Atlantic (12.5 million) but was built up over nearly twice the timespan, i.e. over the period AD 800–1900. Before the establishment of Islam in the 7th century, little or no source material exists.28 Beginning in the 9th century, Arab and Muslim writers left descriptions of the slave trade from Africa to the Middle East and North Africa. Estimates become more reliable after the 16th century, when Europeans entered the trade. From AD 1600 to 1900, Collins estimates the slave trade at about 5.5 million, half that of the trans-Atlantic trade.28 Estimates by Eltis and Richardson over a similar period are smaller, but proportionally the same by route (Figure 2).27 The direction of the trade from AD 800 to 1900 was trans-Saharan primarily (7.3 million), and across the Red Sea (2.4 million).27 The trans-Saharan trade route was particularly difficult. The ‘Moors’ and other Arabs controlled the slave trade and the destinations were North Africa, Arabia, Mesopotamia, Anatolia, Persia and India. Major slave markets in North Africa were in Marrakech, Algiers, Tunis and Cairo. The traveller Ibn Battutah, a near contemporary of Marco Polo, noted in writings of his travels in the mid-14th century that from (West Africa) ‘come excellent slave-girls, eunuchs, and fabrics dyed with saffron.’30 In Arabia, the markets were in Jeddah, Mecca, and Aden and through the straits of Hormuz into the Arabian/Persian gulf. The remaining 2.9 million Africans were moved from the interior of East Africa to the coast and across the Indian Ocean.27 The annual monsoon winds carried trading dhows northeast then
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Figure 2. Estimated volume and routes of the African slave trade after 1500 (reproduced from Atlas of the Transatlantic Slave Trade with permission of Yale University Press).27
south as far as the Malabar coast of India and Sri Lanka (formerly Ceylon). Before the 19th century, the numbers were comparatively small.19 Beginning in the 19th century, the trade centered primarily on the offshore island of Zanzibar, under the control of Omanis. A substantial number of slaves were shipped around the Cape of Good Hope to Brazil. Remnants of the trade along the Indian west coast are reflected by the existence of the Siddi people of Black African descent who today live along the coast north of Mumbai (formerly Bombay) in the states of Gujarat and Hyderabad in India and Makran and Karachi in Pakistan. Another remnant population are the Sri Lankan Kaffirs. The beginnings of the Arab slave trade coincided with the expansion of Islam in the first few centuries AD.19 The holding of other Muslims as slaves was forbidden, so to meet demand slaves were taken during wars of expansion or by trading.30 Slaves came not only from Africa but also from the edges of the Islamic world in every direction, including whites to the north; the Slavs (origin of the term slave) from Eastern Europe and Circassians from the Caucasus (Circassian females were prized for their beauty and sought after as concubines). But most came from sub-Saharan Africa and from along the eastern coast, the Bar-el-Zanj (coast of the blacks). Arab traders ventured to East and Southeast Asia with the spread of Islam to that region, during the Tang (618–907) to Ming (1368–1644) Chinese dynasties. The Chinese and other Asians also came to the East African coast themselves to trade. The Chinese were interested in ivory, rhinoceros horn, leopard skins and tortoise shells, but bought few slaves.28 During the 10th century, an Arab geographer (al-Masudi of Baghdad) wrote that the primary commodity of maritime traders from East Africa to India and China at the time was ivory.31 In the early 19th century, many slaves remained on Zanzibar or nearby islands to work on the increasing numbers of plantations established for growing cloves, coconuts and grain. The end of slave exportation from the eastern coast began with the signing of an abolitionist treaty between the sultan of Zanzibar and the British in 1822. The African diaspora was primarily to the Caribbean, the Americas, the Arabian peninsula and Europe.32 Few if any Afro-descendants are found in the Far East or in Southeast Asia. Today, black and mixed-black people number in the millions in the Americas, while in China, and probably other parts of East
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Eltis and colleagues estimated that about 12.5 million enslaved Africans were shipped from the west coast of Africa across the Atlantic to the Caribbean and later to North and South America. With an average of 304 slaves per ship and as many as 600 in one voyage, 10.7 million disembarked in more than 35 000 voyages.27 The Voyages database starts in 1501 and includes records of voyages until the trade was finally suppressed in the latter half of the 19th century. The data are derived mostly from direct records (ships’ logs archived in port cities of Europe, from Liverpool to Lisbon) and estimates of the total volume are thought to be accurate. For the British, French and Dutch trade and for trade from Spain and Portugal to Brazil after 1750, the authors believe the database accounts for nearly all slave-trading voyages. By 1647–8, the years generally accepted for the first outbreak of yellow fever in the Caribbean and Yucatan Peninsula of Mexico, just over 700 000 slaves had been disembarked in the Americas. By 1761, when the disease was first considered endemic in Havana, for example, almost 5 million Africans had been disembarked.
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Asia, only a few thousand live among a population of more than a billion. Unlike in the Americas or Arabia, China and other countries in the region had sufficient population to meet the needs for large-scale labour-intensive work.
Nature of slavery in the Indian Ocean World
The reason for the absence of a historical introduction of yellow fever into Asia is largely of theoretical or academic interest. Focal outbreaks of yellow fever may have occurred throughout the world in the past (as they may have in the Americas before the first outbreak in Barbados in 1647), but are not recorded.4,22 A search of Indian and Chinese medical history might reveal descriptions of haemorrhagic diseases in Asia that might have been yellow fever, but could also have been many other diseases (Weil’s disease, dengue haemorrhagic fever, Kyasanur forest disease, Crimean–Congo haemorrhagic fever virus or hantavirus variants).The slave trade hypothesis might be questioned by noting that a large number of potentially infected Indian troops left Africa en masse for Asia (the Indian subcontinent) in pre-vaccine days after World War I and endemicity did not follow, but that event hardly compared with the conditions of transportation and pattern of continual reintroduction during the decades-long slave trade to the Americas. The Indian troops were probably aware of the need for shipboard mosquito control. Indian expeditionary forces under British command fought mainly in East Africa,39 while the distribution of yellow fever at that time was largely confined to coastal West Africa.20 The Indian Ocean was the only potential route to Asia for yellow fever in the days before air travel. The arid environment of North Africa, the Arabian peninsula and Mesopotamia and lack of a suitable non-human primate reservoir would not support maintenance of a sylvatic or savannah cycle. These landmasses would have provided a buffer between Africa and suitable yellow fever environments farther to the southeast. But today the potential for direct introduction into tropical regions to the east, where there has been no previous exposure in the population, remains a major public health concern. The recent outbreak in Sudan is a reminder that yellow fever remains a threat nowadays and that outbreaks in East Africa are not uncommon.40 Since the development of a yellow fever vaccine early in the 20th century and institution of mosquito control measures, large-scale yellow fever epidemics are mostly a thing of the past. Smaller outbreaks still occur regularly and are increasing, particularly in Africa; this is in part because of the lack of vaccination in developing countries in endemic areas. Present-day air travel replicates and magnifies the conditions for spread of a virus across vast spaces. However, the size of the mosquito vector population transported via an aircraft and modern disinsection practices probably make this an unlikely, although not impossible, means of sparking an epidemic of yellow fever in a distant land.41 In 1934, Dudley raised the concern that yellow fever might at that time still spread from the eastern coast of Africa to Asia, expressing the possibility of ‘a holocaust to which all the historical epidemics would be as the Battle of Waterloo was to the Great War’.12 The requirement of a yellow fever vaccination certificate by Asian countries for people entering from yellow fever endemic areas provides little guarantee that yellow fever cannot still enter Asia. Shortages of yellow fever vaccine in India for a time presented a problem for individuals traveling to Africa, who are required to have a certificate on return. Fake vaccination certificates have been sold in Kenya42 and Nigeria43 in the past and more recently in India.44 It could be that all the proposed explanations for the lack of yellow fever transmission to Asia before modern understanding
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In one volume of a series of specialist studies on slavery in the Indian Ocean World (considered to range from China to Southeast and South Asia, the Middle East and Africa), Campbell makes it clear that ‘the essential features of the slave-trade and slavery in the Indian Ocean World contrast sharply with those of the trans-Atlantic slave-trade and plantation slavery in the Americas’.33 Most documentation suggests that slaves in Arabia served as domestics, performing menial tasks. Eunuchs were used to guard the harem or serve as custodians in mosques and other important places. However, the impression that most slaves were used primarily in those roles may only reflect the lack of documentation of practices in the countryside in the early years of Islam.30 There is evidence that slaves were used on date plantations, in the mines and in the draining of marshes, activities more on the scale of slavery in the Americas, which required a large manual workforce. Ibn Battutah described salt mining in the western Sahara by slaves owned by Berbers.34 In addition to mining salt in the Sahara, black slaves were used for gold mining in Nubia and the draining of marshes in the lower reaches of the Tigris–Euphrates river.27 One of the largest slave revolts in history occurred in the 9th century among Zanj slaves involved in draining the Mesopotamian marshes.31,35 The Zanj Rebellion, involving half a million African slaves, took place near Basra at the head of the Gulf and lasted for 15 years. Historian Andrew Watson hypothesised the existence of an Arab agricultural revolution in the ‘Fertile Crescent’, the area including the Nile River valley and fertile areas of the Shatt al-Arab around the Tigris–Euphrates river system from the 8th to the 13th century.36 The resulting plantation economy would have required large numbers of slaves to perform the fieldwork. Slaves who converted to Islam were later freed and assimilated into the population (in contrast to the Afro-American experience).30 A substantial portion of the population of countries on the Arabian Peninsula today are of black African or mixed descent. They are Muslim, Arab-speaking and many are in the professions and other positions of high socioeconomic status. In East and Southeast Asia in contrast, the nature of the work of black African slaves was much different. A colony of Arab traders resided in Guangzhou (formerly Canton) at the mouth of the Pearl River near present-day Hong Kong, but slaves were not a primary commodity.37 In Guangzhou, it was fashionable for a time among the wealthy to have blacks as ‘ornamentals’ so to speak— as doormen and guards, and also as concubines and for domestic work—not in the vast numbers for heavy labour as in the Americas and in the Middle East. Needham noted: ‘The Chinese and other Asian nations had been using negro slaves for many centuries, but the fact that their slavery was basically domestic kept the practice within bounds [short of the massive imports for plantation labor that dominated the Atlantic Trade]’.38 Chinese traders went to Africa and traded directly with Arab traders and Africans, but the purchase of slaves was not nearly on the scale as that of Arabs and Europeans.
Discussion
J. T. Cathey and J. S. Marr
of the disease are correct, but individually each was insufficient to account for the disease’s sustained absence from that continent. In epidemic modelling terms, even if the yellow fever virus reached the Asian Far East, the basic reproduction number never reached the threshold value to establish endemicity.45 In contrast, the continuous and voluminous African slave trade to the Americas was sufficient to cause focal epidemics and for yellow fever eventually to become endemic in regions of the tropical world that could sustain the transmission cycle.
Acknowledgements: We thank Drs Thomas Monath and Jack Woodall for critical reviews, Safiyya Mohamed Ali for editorial assistance and David Connell and Reina Tejano for assistance with the images.
14 Mahaffy A., Smithburn K, Hughes T. The distribution of immunity to yellow fever in central and East Africa. Trans R Soc Trop Med Hyg 1946;40:57–82. 15 Ellis BR, Sang RC, Horne KM et al. Yellow fever virus susceptibility of two mosquito vectors from Kenya, East Africa. Trans R Soc Trop Med Hyg 2012;106:387–9. 16 Sanders EJ, Marfin AA, Tukei PM et al. First recorded outbreak of yellow fever in Kenya, 1992–1993. I. Epidemiologic investigations. Am J Trop Med Hyg 1998;59:644–9. 17 Monath TP, Gershman M, Hill DR et al. Yellow fever recommendations for tourists to Kenya: a flawed risk assessment. J Trav Med 2009:16;146; author reply 146–7. 18 McNeill J. Mosquito Empires: Ecology and War in the Greater Caribbean, 1620–1914. Cambridge: Cambridge University Press; 2010. p. 390. 19 Manning P. Slavery and African Life: Occidental, Oriental, and African Slave Trades. Cambridge: Cambridge University Press; 1990. p. 52.
Funding: None.
20 Frierson JG. The yellow fever vaccine: A history. Yale J Biol Med 2010;83:77–85.
Competing interests: None declared.
21 Stitt ER. The Diagnostics and Treatment of Tropical Diseases, 3rd edn, revised. Miami: HardPress Publishing; 1919.
Ethical approval: Not required.
22 Carter HR. Yellow Fever: An epidemiological and historical study of its place of origin. Philadelphia, PA: Williams & Wilkins; 1931. p. 308.
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Authors’ contributions: JC conceived the idea of the review and wrote the manuscript; JM made critical suggestions and contributed to content and writing. Both authors read and approved the final manuscript. JC is guarantor of the paper.
13 Jentes ES, Poumerol G, Gershman MD et al. The revised global yellow fever risk map and recommendations for vaccination, 2010: consensus of the Informal WHO Working Group on Geographic Risk for Yellow Fever. Lancet Infect Dis 2011;11:622–32.
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