Chapter 3 : The Human-Animal Interface

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The human-animal interface is as ancient as the first bipedal steps taken by humans. It has grown and expanded with the human species' prehistoric and historical development to reach the unprecedented scope of current times. Several facets define the human-animal interface, guiding the scope and range of human interactions with animal species. These facets have continued to evolve and expand since their emergence, promoting disease emergence. Placing the human-animal interface in its historical perspective allows us to realize its versatile and dynamic nature. Changes in the scope and range of domestication, agriculture, urbanization, colonization, trade, and industrialization have been accompanied by evolving risks for cross-species transmission of pathogens. Because these risks are unlikely to decrease, improving our technologies to identify and monitor pathogenic threats lurking at the human-animal interface should be a priority.

Citation: Reperant L, M. E. Osterhaus A. 2014. The Human-Animal Interface, p 33-52. In Atlas R, Maloy S (ed), One Health. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.OH-0013-2012

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Figure 1

Schematic of the human-animal interface. The different facets of the human-animal interface include the evolutionary pathogen heritage of the human species and human demographics and behaviors associated with domestication, agriculture and food production, urbanization, worldwide migration, colonization and trade, and industrialization and globalization. These facets interact and expand as mankind continues to develop. doi:10.1128/microbiolspec.OH-0013-2012.f1

Citation: Reperant L, M. E. Osterhaus A. 2014. The Human-Animal Interface, p 33-52. In Atlas R, Maloy S (ed), One Health. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.OH-0013-2012
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Figure 2

Ancestral origins of human pathogens. Most pathogens capable of infecting the human species have originated from animal pathogens that crossed the species barrier, in particular across the domesticated human-animal interface. Human viruses belonging to 32 different genera have their ancestral origins in animal precursors and have adapted to efficiently transmit among humans (light pink), while viruses belonging to 37 different genera are zoonotic pathogens with no or limited ability to transmit among humans (dark pink). The remaining pathogens are heirloom pathogens that cospeciated with the human species. Of these, viruses belonging to 16 different genera were vertically transmitted from hominin ancestral species at the emergence of the genus (dark blue), while viruses belonging to 6 different genera were vertically transmitted from related spp. to the modern human at the time of its emergence (light blue). doi:10.1128/microbiolspec.OH-0013-2012.f2

Citation: Reperant L, M. E. Osterhaus A. 2014. The Human-Animal Interface, p 33-52. In Atlas R, Maloy S (ed), One Health. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.OH-0013-2012
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Figure 3

Evidence of smallpox infection of Pharaoh Ramses V. Poxlike lesions reminiscent of smallpox pustules can be seen on the head of the 3,000-year-old mummy. Source: World Health Organization. doi:10.1128/microbiolspec.OH-0013-2012.f3

Citation: Reperant L, M. E. Osterhaus A. 2014. The Human-Animal Interface, p 33-52. In Atlas R, Maloy S (ed), One Health. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.OH-0013-2012
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Figure 4

Diversity of avian and swine influenza viruses. The annual productions of swine and poultry meat have dramatically increased since the 1960s (upper and lower panel, connected dots). Concurrently, the number of new influenza virus lineages in swine (upper panel, black bars) and the number of outbreaks of highly pathogenic avian influenza in poultry (lower panel, black bars) have increased similarly since the discovery of the virus in pigs in the 1930s and in poultry in the 1950s. These increases in viral diversity have been accompanied by an increase in the number of swine and avian influenza virus subtypes or lineages that have caused infection in humans (upper and lower panels, gray bars). Modified from reference . doi:10.1128/microbiolspec.OH-0013-2012.f4

Citation: Reperant L, M. E. Osterhaus A. 2014. The Human-Animal Interface, p 33-52. In Atlas R, Maloy S (ed), One Health. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.OH-0013-2012
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1. Reperant LA,, Cornaglia G,, Osterhaus AD . 2012. The importance of understanding the human-animal interface: from early hominins to global citizens. Curr Top Microbiol Immunol [Epub ahead of print.] doi:10.1007/82_2012_269. [PubMed] [CrossRef]
2. Herfst S,, Schrauwen EJ,, Linster M,, Chutinimitkul S,, de Wit E,, Munster VJ,, Sorrell EM,, Bestebroer TM,, Burke DF,, Smith DJ,, Rimmelzwaan GF,, Osterhaus AD,, Fouchier RA . 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336 : 15341541. [PubMed] [CrossRef]
3. Imai M,, Watanabe T,, Hatta M,, Das SC,, Ozawa M,, Shinya K,, Zhong G,, Hanson A,, Katsura H,, Watanabe S,, Li C,, Kawakami E,, Yamada S,, Kiso M,, Suzuki Y,, Maher EA,, Neumann G,, Kawaoka Y . 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486 : 420428. [PubMed] [CrossRef]
4. Russell CA,, Fonville JM,, Brown AE,, Burke DF,, Smith DL,, James SL,, Herfst S,, van Boheemen S,, Linster M,, Schrauwen EJ,, Katzelnick L,, Mosterin A,, Kuiken T,, Maher E,, Neumann G,, Osterhaus AD,, Kawaoka Y,, Fouchier RA,, Smith DJ . 2012. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336 : 15411547. [PubMed] [CrossRef]
5. Van Blerkom LM . 2003. Role of viruses in human evolution. Am J Phys Anthropol 122(Suppl 37): 1446. [PubMed] [CrossRef]
6. Gagneux S . 2012. Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci 367 : 850859. [PubMed] [CrossRef]
7. Ollomo B,, Durand P,, Prugnolle F,, Douzery E,, Arnathau C,, Nkoghe D,, Leroy E,, Renaud F . 2009. A new malaria agent in African hominids. PLoS Pathog 5 : e1000446. [PubMed] [CrossRef]
8. Stevens JR,, Gibson W . 1999. The molecular evolution of trypanosomes. Parasitol Today 15 : 432437. [PubMed]
9. Weiss RA . 2009. Apes, lice and prehistory. J Biol 8 : 20. [PubMed] [CrossRef]
10. Hoberg EP,, Alkire NL,, de Queiroz A,, Jones A . 2001. Out of Africa: origins of the Taenia tapeworms in humans. Proc Biol Sci 268 : 781787. [PubMed] [CrossRef]
11. Linz B,, Balloux F,, Moodley Y,, Manica A,, Liu H,, Roumagnac P,, Falush D,, Stamer C,, Prugnolle F,, van der Merwe SW,, Yamaoka Y,, Graham DY,, Perez-Trallero E,, Wadstrom T,, Suerbaum S,, Achtman M . 2007. An African origin for the intimate association between humans and Helicobacter pylori . Nature 445 : 915918. [PubMed] [CrossRef]
12. McGeoch DJ,, Dolan A,, Ralph AC . 2000. Toward a comprehensive phylogeny for mammalian and avian herpesviruses. J Virol 74 : 1040110406. [PubMed]
13. McGeoch DJ,, Rixon FJ,, Davison AJ . 2006. Topics in herpesvirus genomics and evolution. Virus Res 117 : 90104. [PubMed] [CrossRef]
14. King AA,, Shrestha S,, Harvill ET,, Bjornstad ON . 2009. Evolution of acute infections and the invasion-persistence trade-off. Am Nat 173 : 446455. [PubMed] [CrossRef]
15. Bartlett MJ . 1957. Measles periodicity and community size. J R Statist Soc A 120 : 4870.
16. Diamond J . 2002. Evolution, consequences and future of plant and animal domestication. Nature 418 : 700707. [PubMed] [CrossRef]
17. Wolfe ND,, Dunavan CP,, Diamond J . 2007. Origins of major human infectious diseases. Nature 447 : 279283. [PubMed]
18. Hare R, . 1967. The antiquity of diseases caused by bacteria and viruses: a review of the problem from a bacteriologist's point of view, p 115131. In Brothwell D,, Sandison AT (ed), Diseases in Antiquity. Charles C Thomas, Publisher, Springfield, IL.
19. Comas I,, Gagneux S . 2009. The past and future of tuberculosis research. PLoS Pathog 5 : e1000600. [PubMed] [CrossRef]
20. Roca AL,, Pecon-Slattery J,, O’Brien SJ . 2004. Genomically intact endogenous feline leukemia viruses of recent origin. J Virol 78 : 43704375. [PubMed]
21. Kapoor A,, Simmonds P,, Gerold G,, Qaisar N,, Jain K,, Henriquez JA,, Firth C,, Hirschberg DL,, Rice CM,, Shields S,, Lipkin WI . 2011. Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci USA 108 : 1160811613. [PubMed] [CrossRef]
22. de Graaf M,, Osterhaus AD,, Fouchier RA,, Holmes EC . 2008. Evolutionary dynamics of human and avian metapneumoviruses. J Gen Virol 89 : 29332942. [PubMed] [CrossRef]
23. Allander T,, Tammi MT,, Eriksson M,, Bjerkner A,, Tiveljung-Lindell A,, Andersson B . 2005. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci USA 102 : 1289112896. [PubMed] [CrossRef]
24. McIntosh K . 2006. Human bocavirus: developing evidence for pathogenicity. J Infect Dis 194 : 11971199. [PubMed] [CrossRef]
25. Taubenberger JK,, Morens DM . 2006. 1918 influenza: the mother of all pandemics. Emerg Infect Dis 12 : 1522. [PubMed] [CrossRef]
26. Parrish CR,, Kawaoka Y . 2005. The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59 : 553586. [PubMed] [CrossRef]
27. Chomel BB,, Belotto A,, Meslin FX . 2007. Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 13 : 611. [PubMed] [CrossRef]
28. Wolfe ND,, Daszak P,, Kilpatrick AM,, Burke DS . 2005. Bushmeat hunting, deforestation, and prediction of zoonoses emergence. Emerg Infect Dis 11 : 18221827. [PubMed]
29. Peiris JS,, Yuen KY,, Osterhaus AD,, Stohr K . 2003. The severe acute respiratory syndrome. N Engl J Med 349 : 24312441. [PubMed] [CrossRef]
30. Zaki AM,, van Boheemen S,, Bestebroer TM,, Osterhaus AD,, Fouchier RA . 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367 : 18141820. [PubMed] [CrossRef]
31. Chua KB . 2003. Nipah virus outbreak in Malaysia. J Clin Virol 26 : 265275. [PubMed]
32. Charrel RN,, de Lamballerie X . 2003. Arenaviruses other than Lassa virus. Antiviral Res 57 : 89100. [PubMed]
33. Zeier M,, Handermann M,, Bahr U,, Rensch B,, Muller S,, Kehm R,, Muranyi W,, Darai G . 2005. New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention—a review. Virus Genes 30 : 157180. [PubMed] [CrossRef]
34. Achtman M,, Zurth K,, Morelli G,, Torrea G,, Guiyoule A,, Carniel E . 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis . Proc Natl Acad Sci USA 96 : 1404314048. [PubMed]
35. Perry RD,, Fetherston JD . 1997. Yersinia pestis—etiologic agent of plague. Clin Microbiol Rev 10 : 3566. [PubMed]
36. Field HE,, Mackenzie JS,, Daszak P, . 2007. Henipaviruses: emerging paramyxoviruses associated with fruit bats, p 133159. In Childs JE,, Mackenzie JS,, Richt JA (ed), Wildlife and Emerging Zoonotic Diseases: the Biology, Circumstances and Consequences of Cross-Species Transmission. Springer, Berlin, Germany.
37. Bradley CA,, Altizer S . 2007. Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22 : 95102. [PubMed] [CrossRef]
38. Hopkins D . 1980. Ramses V: earliest known victim? World Health 5 : 22 http://whqlibdoc.who.int/smallpox/WH_5_1980_p22.pdf (last accessed May 2, 2013).
39. Larsen CS . 2006. The agricultural revolution as environmental catastrophe: implications for health and lifestype in the Holocene. Quat Int 150 : 1220.
40. McCormick M . 2003. Rats, communications, and plague: toward an ecological history. J Interdiscipl Hist 34 : 125.
41. Papagrigorakis MJ,, Yapijakis C,, Synodinos PN, . 2008. Typhoid fever epidemic in ancient Athens, p 161173. In Raoult D,, Drancourt M (ed), Paleomicrobiology: Past Human Infections. Springer, Berlin, Germany.
42. Yusim K,, Peeters M,, Pybus OG,, Bhattacharya T,, Delaporte E,, Mulanga C,, Muldoon M,, Theiler J,, Korber B . 2001. Using human immunodeficiency virus type 1 sequences to infer historical features of the acquired immune deficiency syndrome epidemic and human immunodeficiency virus evolution. Philos Trans R Soc Lond B Biol Sci 356 : 855866. [PubMed] [CrossRef]
43. Heeney JL,, Dalgleish AG,, Weiss RA . 2006. Origins of HIV and the evolution of resistance to AIDS. Science 313 : 462466. [PubMed] [CrossRef]
44. Bar-Yosef O,, Belfer-Cohen A . 2001. From Africa to Eurasia—early dispersals. Quat Int 75 : 1928.
45. de Thé G . 2007. Microbial genomes to write our history. J Infect Dis 196 : 499501. [PubMed] [CrossRef]
46. Slattery JP,, Franchini G,, Gessain A . 1999. Genomic evolution, patterns of global dissemination, and interspecies transmission of human and simian T-cell leukemia/lymphotropic viruses. Genome Res 9 : 525540. [PubMed]
47. Verdonck K,, Gonzalez E,, Van Dooren S,, Vandamme AM,, Vanham G,, Gotuzzo E . 2007. Human T-lymphotropic virus 1: recent knowledge about an ancient infection. Lancet Infect Dis 7 : 266281. [PubMed] [CrossRef]
48. Wheelis M . 2002. Biological warfare at the 1346 siege of Caffa. Emerg Infect Dis 8 : 971975. [PubMed] [CrossRef]
49. Acemoglu D,, Robinson J,, Johnson S . 2003. Disease and development in historical perspective. J Eur Econ Assoc 1 : 397405.
50. Diamond J . 1999. Guns, Germs, and Steel: the Fates of Human Societies. W. W. Norton & Company, New York, NY.
51. Curtin PD . 1968. Epidemiology and the slave trade. Polit Sci Q 83 : 190216. [PubMed]
52. Timen A,, Koopmans MP,, Vossen AC,, van Doornum GJ,, Gunther S,, van den Berkmortel F,, Verduin KM,, Dittrich S,, Emmerich P,, Osterhaus AD,, van Dissel JT,, Coutinho RA . 2009. Response to imported case of Marburg hemorrhagic fever, The Netherlands. Emerg Infect Dis 15 : 11711175. [PubMed] [CrossRef]
53. van Thiel PP,, van den Hoek JA,, Eftimov F,, Tepaske R,, Zaaijer HJ,, Spanjaard L,, de Boer HE,, Van Doornum GJ,, Schutten M,, Osterhaus AD,, Kager PA . 2007. Fatal case of human rabies (Duvenhage virus) from a bat in Kenya: The Netherlands, December 2007. Euro Surveill 13 :pii=8007.
54. Khan K,, Arino J,, Hu W,, Raposo P,, Sears J,, Calderon F,, Heidebrecht C,, Macdonald M,, Liauw J,, Chan A,, Gardam M . 2009. Spread of a novel influenza A (H1N1) virus via global airline transportation. N Engl J Med 361 : 212214. [PubMed] [CrossRef]
55. Russell CA,, Jones TC,, Barr IG,, Cox NJ,, Garten RJ,, Gregory V,, Gust ID,, Hampson AW,, Hay AJ,, Hurt AC,, de Jong JC,, Kelso A,, Klimov AI,, Kageyama T,, Komadina N,, Lapedes AS,, Lin YP,, Mosterin A,, Obuchi M,, Odagiri T,, Osterhaus AD,, Rimmelzwaan GF,, Shaw MW,, Skepner E,, Stohr K,, Tashiro M,, Fouchier RA,, Smith DJ . 2008. The global circulation of seasonal influenza A (H3N2) viruses. Science 320 : 340346. [PubMed] [CrossRef]
56. Grenfell BT,, Bjornstad ON,, Kappey J . 2001. Travelling waves and spatial hierarchies in measles epidemics. Nature 414 : 716723. [PubMed] [CrossRef]
57. Viboud C,, Bjornstad ON,, Smith DL,, Simonsen L,, Miller MA,, Grenfell BT . 2006. Synchrony, waves, and spatial hierarchies in the spread of influenza. Science 312 : 447451. [PubMed] [CrossRef]
58. Rosenthal BM . 2009. How has agriculture influenced the geography and genetics of animal parasites? Trends Parasitol 25 : 6770. [PubMed] [CrossRef]
59. Mills JN,, Childs JE . 1998. Ecologic studies of rodent reservoirs: their relevance for human health. Emerg Infect Dis 4 : 529537. [PubMed] [CrossRef]
60. Lin XD,, Guo WP,, Wang W,, Zou Y,, Hao ZY,, Zhou DJ,, Dong X,, Qu YG,, Li MH,, Tian HF,, Wen JF,, Plyusnin A,, Xu J,, Zhang YZ . 2012. Migration of Norway rats resulted in the worldwide distribution of Seoul hantavirus today. J Virol 86 : 972981. [PubMed] [CrossRef]
61. Normile D . 2008. Rinderpest. Driven to extinction. Science 319 : 16061609. [PubMed] [CrossRef]
62. Blancou J . 2002. History of the control of foot and mouth disease. Comp Immunol Microbiol Infect Dis 25 : 283296. [PubMed]
63. Knudsen AB . 1995. Global distribution and continuing spread of Aedes albopictus . Parassitologia 37 : 9197. [PubMed]
64. Rappole JH,, Derrickson SR,, Hubalek Z . 2000. Migratory birds and spread of West Nile virus in the Western Hemisphere. Emerg Infect Dis 6 : 319328. [PubMed] [CrossRef]
65. Di Giulio DB,, Eckburg PB . 2004. Human monkeypox: an emerging zoonosis. Lancet Infect Dis 4 : 1525. [PubMed]
66. Gibbens JC,, Sharpe CE,, Wilesmith JW,, Mansley LM,, Michalopoulou E,, Ryan JB,, Hudson M . 2001. Descriptive epidemiology of the 2001 foot-and-mouth disease epidemic in Great Britain: the first five months. Vet Rec 149 : 729743. [PubMed]
67. Thompson D,, Muriel P,, Russell D,, Osborne P,, Bromley A,, Rowland M,, Creigh-Tyte S,, Brown C . 2002. Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001. Rev Sci Tech 21 : 675687. [PubMed]
68. Daszak P,, Cunningham AA,, Hyatt AD . 2000. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287 : 443449. [PubMed]
69. Weldon C,, du Preez LH,, Hyatt AD,, Muller R,, Spears R . 2004. Origin of the amphibian chytrid fungus. Emerg Infect Dis 10 : 21002105. [PubMed] [CrossRef]
70. Frick WF,, Pollock JF,, Hicks AC,, Langwig KE,, Reynolds DS,, Turner GG,, Butchkoski CM,, Kunz TH . 2010. An emerging disease causes regional population collapse of a common North American bat species. Science 329 : 679682. [PubMed] [CrossRef]
71. Bengis RG,, Kock RA,, Fischer J . 2002. Infectious animal diseases: the wildlife/livestock interface. Rev Sci Tech 21 : 5365. [PubMed]
72. Gilbert M,, Xiao X,, Chaitaweesub P,, Kalpravidh W,, Premashthira S,, Boles S,, Slingenbergh J . 2007. Avian influenza, domestic ducks and rice agriculture in Thailand. Agric Ecosyst Environ 119 : 409415. [PubMed] [CrossRef]
73. Scholtissek C,, Naylor E . 1988. Fish farming and influenza pandemics. Nature 331 : 215. [PubMed] [CrossRef]
74. Tully DC,, Fares MA . 2008. The tale of a modern animal plague: tracing the evolutionary history and determining the time-scale for foot and mouth disease virus. Virology 382 : 250256. [PubMed] [CrossRef]
75. Reperant LA,, Osterhaus AD, . 2012. Avian and animal influenza, p 3139. In Van-Tam J,, Sellwood C (ed), Pandemic Influenza, 2nd ed. CABI, Wallingford, United Kingdom.
76. Brown P,, Will RG,, Bradley R,, Asher DM,, Detwiler L . 2001. Bovine spongiform encephalopathy and variant Creutzfeldt-Jakob disease: background, evolution, and current concerns. Emerg Infect Dis 7 : 616. [PubMed] [CrossRef]
77. Gold HS,, Moellering RC, Jr . 1996. Antimicrobial-drug resistance. N Engl J Med 335 : 14451453. [PubMed] [CrossRef]
78. Patz JA,, Epstein PR,, Burke TA,, Balbus JM . 1996. Global climate change and emerging infectious diseases. JAMA 275 : 217223. [PubMed]
79. Rogers DJ,, Randolph SE . 2006. Climate change and vector-borne diseases. Adv Parasitol 62 : 345381. [PubMed] [CrossRef]
80. Davies J . 2013. Antibiotic resistance in and from nature. Microbiol Spectrum 1(1): OH-0005-2012. doi:10.1128/microbiolspec.OH-0005-2012.

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