The Animal-Human Interface and Infectious Disease in Industrial Food Animal Production: Rethinking Biosecurity and Biocontainment

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1 Prctice Articles The Animl-Humn Interfce nd Infectious Disese in Industril Food Animl Production: Rethinking Biosecurity nd Biocontinment Jy P. Grhm, PhD Jessic H. Leibler, MS Lnce B. Price, PhD Jochim M. Otte, DVM b Dirk U. Pfeiffer, DVM c T. Tiensin, DVM d Ellen K. Silbergeld, PhD SYNOPSIS Understnding interctions between nimls nd humns is criticl in preventing outbreks of zoonotic disese. This is prticulrly importnt for vin influenz. Food niml production hs been trnsformed since the 1918 influenz pndemic. Poultry nd swine production hve chnged from smllscle methods to industril-scle opertions. There is substntil evidence of pthogen movement between nd mong these industril fcilities, relese to the externl environment, nd exposure to frm workers, which chllenges the ssumption tht modern poultry production is more biosecure nd biocontined s compred with bckyrd or smll holder opertions in preventing introduction nd relese of pthogens. An nlysis of dt from the Thi government investigtion in 2004 indictes tht the odds of H5N1 outbreks nd infections were significntly higher in lrge-scle commercil poultry opertions s compred with bckyrd flocks. These dt suggest tht successful strtegies to prevent or mitigte the emergence of pndemic vin influenz must consider risk fctors specific to modern industrilized food niml production. Johns Hopkins Bloomberg School of Public Helth, Deprtment of Environmentl Helth Sciences, Division of Environmentl Helth Engineering, Bltimore, MD b Food nd Agriculture Orgniztion Animl Production nd Helth Division, Rome, Itly c Epidemiology Division, Deprtment of Veterinry Clinicl Sciences, Royl Veterinry College, Htfield, Hertfordshire, UK d Fculty of Veterinry Medicine, Utrecht University, Utrecht, The Netherlnds Address correspondence to: Ellen K. Silbergeld, PhD, Johns Hopkins Bloomberg School of Public Helth, Deprtment of Environmentl Helth Sciences, Division of Environmentl Helth Engineering, 615 N. Wolfe St., Room E6644, Bltimore, MD 21205; tel ; fx ; e-mil <esilberg@jhsph.edu> Assocition of Schools of Public Helth 282

2 Infectious Disese in Industril Food Animl Production 283 The emergence nd spred of vin influenz viruses re complex nd incompletely understood. 1 While preprtion for pndemic disese is criticlly importnt public helth tsk, understnding risk fctors for disese trnsmission t the niml-humn interfce my identify opportunities for disese prevention nd outbrek continment. There is gret interest in exmining decisive events in the 1918 pndemic experience to inform plnning. 2 These studies hve highlighted the significnce of domesticted species in the development nd emergence of highly pthogenic vin influenz (HPAI) virus nd strins tht re trnsmissible to humns. The source of initil humn exposure in 1918 remins uncertin, nd it is not cler if interspecies trnsmission ws necessrily involved in virl ressortment, which could hve occurred in settings where swine, chickens, nd humns coexisted in close contct. 3,4 Recent studies hve presented evidence for nd ginst genetic ressortment tht is suggestive of modifiction in the course of interspecies trnsmission. 5 Since 1918, much hs chnged in the reltionships between humn popultions nd domesticted food nimls, including poultry nd swine. It is often ssumed tht modern methods of intensive food niml production provide incresed biosecurity nd biocontinment nd thus reduced risks for trnsfers of zoonotic disese to humns, but these ssumptions need to be criticlly exmined. This rticle undertkes three objectives: (1) review of the chnges in food niml production tht hve occurred over the pst century worldwide, with focus on spects of biosecurity nd biocontinment t the niml-humn interfce; (2) evidence from studies of other pthogen movement from confined poultry nd swine opertions resulting in environmentl releses, interspecies trnsmission, nd opportunities for humn infection; nd (3) n nlysis of dt from the Thi government progrm of H5N1 surveillnce nd outbrek investigtions. TRANSFORMATION OF FOOD ANIMAL PRODUCTION Over the pst 70 yers, food niml production in much of the world, beginning in the U.S., hs been trnsformed from trditionl smll-scle methods nd entrepreneuril orgniztion to industril-scle opertions nd verticlly integrted mngement in which most if not ll spects of production (breeding, supply of young nimls, feeds, niml husbndry) re controlled by single entity. 6,7 Both of these chrcteristics re relevnt to understnding the current nture of the niml-humn interfce. Industril or lrge-scle food niml production (IFAP) involves high throughput niml husbndry, in which thousnds of nimls of one breed nd for one purpose (i.e., pigs, lyer hens, broiler chickens, ducks, turkeys, beef or diry cttle, finfish, or crustce) re rised with short-genertion intervls t single sites under highly controlled conditions, often in confined housing, with defined feeds replcing ccess to forge crops. These methods fcilitte the uniform nd relible production of consumer products through stremlined orgniztionl nd production structure, improvements in breeding nd niml husbndry, incresed veterinry oversight, nd specilly formulted diets, including the ddition of ntibiotics to promote feed conversion efficiency nd growth rtes. 8,9 In the U.S., these fcilities re known s niml feeding opertions (AFOs). Concentrted AFOs (CAFOs) re type of AFO tht hs regultory definition s fcilities tht hve nimls stbled or confined for t lest 45 dys out of ny 12-month period nd holding t lest 1,000 niml units (AUs) (1 AU 5 1,000 pounds). In the U.S., this chnge begn in the 1930s nd now more thn 90% of broiler chickens nd turkeys re produced in houses in which between 15,000 nd 50,000 birds re confined throughout their lifespn. For swine, this trnsformtion occurred more recently nd more rpidly: from 1994 to 2001, the mrket shre of hogs produced in IFAP incresed from 10% to 72% of totl U.S. production. 10 The chnge to n industril model of production hs lso reduced frmer utonomy, s most decisions relted to feeding nd housing re determined by the lrge producers (or integrtors) with which frmers or growers contrct to rise nimls. Industril-scle poultry production is expnding rpidly in Asi, Afric, Ltin Americ, North Afric, nd the Ner Est (Tble 1). 11,12 Concerns hve been rised over the reltively wek veterinry nd public helth infrstructure in some of these countries. 13 Swine production is lso incresing; for exmple, in Chin, pork production incresed from 42 million tons to 51 million tons from 2001 to This increse is lrgely relted to the expnsion of the integrted or industril model of production 14 led by both ntionl nd multintionl corportions for expnding mrkets of incresingly urbn consumer popultions within these countries s well s exports. 11 The economic consolidtion of poultry nd swine production hs lso ffected the geogrphy of food niml popultions. Over the pst 60 yers, the geogrphic distribution of both swine nd poultry production in the U.S. hs shrunk, with poultry production now highly concentrted in the southestern sttes nd hog

3 284 Prctice Articles Tble 1. Growth of poultry met production in selected countries, ,b Country/region United Sttes 14,033 14,696 15,792 Chin 9,278 9,898 10,200 Brzil 6,567 7,645 9,080 Europen Union c 7,883 7,439 7,670 Mexico 2,067 2,290 2,510 Indi 1,250 1,500 1,900 Jpn 1,074 1,127 1,130 Argentin ,080 Cnd ,000 Thilnd 1,230 1, Mlysi Totl 45,992 48,449 52,208 Slingenbergh JI, Gilbert M, de Blogh KI, Wint W. Ecologicl sources of zoonotic diseses. Rev Sci Tech 2004;23: b Production figures re in thousnds of metric tons per yer. c Dt represents EU-25. production concentrted in some of these sme sttes, s well s in the Midwest (Figure 1). Similr trends hve occurred worldwide ccording to the U.S. Deprtment of Agriculture (USDA). 15 For exmple, pig nd poultry densities re highly loclized nd often coincident in the U.S. (Figure 1) nd Asi (Figure 1b). 16 This geogrphic intensity nd coincidence increses the possibility for direct or indirect interctions between lrge popultions of confined poultry nd pigs, with potentil consequences for the development nd trnsmission of some zoonotic diseses between these species nd evolution of pthogens tht re trnsmissible to humns. 17,18 As n exmple, interctions between poultry flocks nd swine herds were documented in cse-control study of the outbrek of clssicl swine fever in the Netherlnds. 19 ANIMAL-HUMAN INTERFACES IN IFAP: LIMITS OF BIOSECURITY AND BIOCONTAINMENT These new modes of poultry nd swine production hve chnged the nture of the niml-humn interfce in both griculture nd the surrounding environment, with importnt implictions for zoonotic diseses nd biosecurity more generlly. Biosecurity is defined s ny prctice or system tht prevents the spred of infectious gents from infected to susceptible nimls, or prevents the introduction of infected nimls into herd, region, or country in which the infection hs not yet occurred. 20 Another, more strict definition of biosecurity is the outcome of ll ctivities undertken by n entity to preclude the introduction of disese gents into n re tht one is trying to protect, while biocontinment is the effort tken to prevent spred of disese within herd or flock when the disese is lredy present. 21 This definition cn be extended to include mesures for preventing relese of pthogens from n infected herd. Although combintion of mesures my significntly reduce the risk of pthogen introduction nd relese, for vriety of pthogens zero risk is virtully impossible to chieve in frmed livestock popultions, even in highly developed country settings. Prcticl implementtion of biosecurity nd biocontinment requires mesures to be tilored to the pthogens tht constitute the thret, s well s to the production prctices of the frming system t risk. This requires identifiction of the min pthwys of pthogen trnsmission, quntifiction of risks nd ssessment of efficcy, nd cost of proposed risk mitigtion mesures. Given the focus of this rticle, we illustrte significnt pthwys of pthogen trnsmission tht re intensified by industril food niml production nd remin lrgely unddressed by current prevention mesures. Occuptionl pthwys While fewer people re now engged in niml husbndry t fewer sites (s shown in Figure 2 for hog production in the U.S.), the high throughput nd confinement of highly concentrted niml popultions increses the intensity of microbil exposures for frmers, their fmilies, frm workers, veterinrins, nd others in contct with these opertions. In the U.S., s in much of the world, there is little regultion of occuptionl conditions or worker exposures in most high-density niml houses. The conditions of work, s illustrted in Figure 3, provide mny opportunities for both worker infection nd trnsfer to others in the community. With the exception of concerns bout disposl of ded chickens during n outbrek, 22 there hs been miniml ttention to niml-humn interctions ssocited with the opertion nd mngement of broiler poultry houses. Mny workers re provided little or no protective clothing or opportunities for personl hygiene or decontmintion on-site. Our studies of poultry house workers in Mrylnd indicte tht workers tke their clothes home for wshing. 23 Thus, it is not surprising tht incresed risks of pthogen exposure nd infections, both bcteril nd virl, hve been reported mong frmers, their fmilies, nd frm workers t poultry nd swine opertions

4 Infectious Disese in Industril Food Animl Production 285 Figure 1. Dot density mps of swine nd broiler production in the U.S. in 2002 United Sttes Deprtment of Agriculture census of griculture [cited 2008 Jn 21]. Avilble from: URL: reserch/tls02/tls-livestock.html

5 286 Prctice Articles Figure 1b. Density distribution mps of swine nd poultry in Asi estimted for Gerber P, Chilond P, Frnceschini G, Menzi H. Geogrphicl determinnts nd environmentl implictions of livestock production intensifiction in Asi. Bioresour Technol 2005;96:

6 Infectious Disese in Industril Food Animl Production 287 Figure 2. Temporl trends in the number of hog opertions nd number of hogs per opertion in the U.S., Myers KP, Olsen CW, Setterquist SF, Cpuno AW, Donhm KJ, Thcker EL, et l. Are swine workers in the United Sttes t incresed risk of infection with zoonotic influenz virus? Clin Infect Dis 2006;42: Environmentl pthwys In ddition, the design nd opertionl requirements of lrge-scle swine nd broiler poultry houses result in other compromises of biosecurity, s shown schemticlly in Figure 4. Through these multiple pthwys, pthogens move in nd out of CAFOs nd re then vilble for exchnge mong wild vins, domestic vins, swine, nd other nimls s well s humns. Flock size, number of houses, use of untreted wter, nd disposl of poultry wstes on the frm ll increse risks of Cmpylobcter spp. coloniztion of poultry flocks. 34 Moreover, becuse confinement of thousnds of nimls requires controls to reduce het nd regulte humidity, poultry nd swine houses re ventilted with high-volume fns tht result in considerble movement of mterils into the externl environment. 35,36 In 2004, in British Columbi, Cnd, the rpid spred of vin influenz mong poultry flocks ws prtly ttributed to ir exchnges between confinement fcilities locted within severl hundred meters of one nother, highlighting the potentil for dissemintion of HPAI viruses in ir emissions. 36 Tunnel ventiltion systems, which re incresingly used in the U.S. industry, consist of eight 1-meter-dimeter fns positioned t one end of the building. These fns generte lrge quntities of erosolized dust such tht emissions of smll prticles (,10 micrometers in size) from broiler houses cn rnge from 25 to 40 g/m 3 /24 hours, representing million-fold increse s compred with ir smpled in semirurl re. 36 This spect of IFAP hs not been previously noted in studies tht hve ssumed benefits of confining domestic vin popultions in terms of reducing risks of vin influenz. 37 Other points of relese nd interspecies trnsfers include methods of hndling niml house wstes (s discussed lter in this rticle), the use of poultry house wstes in quculture, nd open-truck trnsport of food nimls from frms to processing plnts. Pthogen contmintion of shipping continers nd trucks, which re not enclosed, is known to occur, nd niml stress during trnsport increses pthogen shedding. 38 The role of food niml wstes in interrupting biosecurity In ddition to the production of nimls for humn consumption, IFAP lso produces lrge mounts of niml wste, or biosolids. Animl biosolids contin rnge of pthogens tht my include influenz

7 288 Prctice Articles viruses, which cn persist for extended periods of time in the bsence of specific tretment. The volume of niml wstes is significnt, reflecting the considerble expnsion of food niml production globlly. 39 In the U.S., it is estimted tht 238,000 CAFOs produce 314 million metric tons of wste per yer, which is 100 times s much biosolids produced by treting humn wstewter. 40 Globl estimtes suggest tht 140 million metric tons of poultry litter nd 460 million metric tons of swine wste were produced in 2003 bsed on dt from the Food nd Agriculture Orgniztion. 41,42 Furthermore, becuse of the regionl concentrtion of poultry nd swine production, the genertion of these biosolids is lso highly concentrted geogrphiclly. Workers involved in removing the wstes from niml houses, trnsporting wstes, nd spreding wstes on lnd re especilly t risk of exposure to pthogens through inhltion, derml contct, nd hnd-to-mouth trnsfers. 43 In contrst to the mngement of humn biosolids, 44 there re reltively few regultions for niml wste disposl nd no specific requirements for tretment. Aprt from some use in niml feeds nd quculture, poultry nd swine wstes re lmost entirely mnged by lnd disposl. Pthogens cn survive in untreted nd lnd-disposed wstes from food nimls for Figure 3. Chicken ctchers t work in poultry concentrted niml feeding opertion, U.S., 1999 The Wshington Post. Photo by Frnk Johnston. Reprinted with permission.

8 Infectious Disese in Industril Food Animl Production 289 Figure 4. A schemtic representtion (not to scle) of multiple potentil pthwys for exposure to nd trnsfer of pthogens within the environs of concentrted niml feeding opertions (Artist: Slvdor Senz) Compromises to biosecurity include: (1) workers lcking protective clothing or opportunities for personl hygiene or decontmintion on-site; (2) indequte mngement of niml biosolids, often pplied to lnd without tretment; (3) flies nd other insects tht crry pthogens in nd out of fcilities through ventiltion systems nd smll openings; (4) ventiltion with high-volume fns resulting in considerble movement of mterils into the externl environment; nd (5) trnsporting nimls in open trucks or continers to the frm or for processing. extended periods of time between two nd 12 months for bcteri nd between three nd six months for viruses. 40 Contmintion of both surfce nd ground wter cn result from these prctices. 45 Moreover, both holding nd lnd disposl of poultry wstes cn ttrct wild vins becuse spilled feed is present in these wstes. This is prticulrly likely in the vicinity of their stopover res, such s Gungdong Province in Chin nd the Delmrv Peninsul in the U.S., where wterfowl commonly forge in fields ner poultry production fcilities. In ddition, there is growing use of poultry nd duck house wstes for use in lnd-bsed quculture opertions (e.g., tilpi nd ctfish) in mny countries (either in integrted fcilities, s in Asi nd Afric, or fter processing, s in the Europen Union nd the U.S.) This mode of pthogen trnsfer is wholly unregulted. Open impoundments for quculture re essentilly smll wetlnds, nd they re frequently visited by wild vins, setting up nother setting for bidirectionl pthogen trnsfers. It should be noted tht the fecl-wter-orl route is considered highly probble mode of trnsmission of vin influenz virus between birds. 49

9 290 Prctice Articles Evidence from studies of niml-humn nd niml-niml trnsfers of bcteri in IFAP There is pucity of reserch on trnsfers of viruses from IFAP; however, there is extensive literture on the exchnge of bcteri mong confined food nimls, wild nimls, humns, nd the environment. This literture supports concerns bout the efficcy of biocontinment t industril food niml production opertions. Reserch on Cmpylobcter spp. is prticulrly relevnt in this regrd, s Cmpylobcter is n vin commensl tht frequently colonizes commercil broiler flocks. In humns, Cmpylobcter cuses serious dirrhel disese (cmpylobcteriosis) of considerble public helth significnce. 23 As for vin influenzs, wild birds re the nturl vertebrte reservoirs of Cmpylobcter, nd they cn serve s vectors for trnsmission to other vertebrtes Cmpylobcter moves mong vin host species, both domesticted 57 nd wild, nd the exchnge of Cmpylobcter between broiler flocks nd wild vins cn occur in both directions. 61 There re severl pthwys for Cmpylobcter coloniztion of broiler flocks including in ovo verticl trnsmission, crryover from previous flocks, horizontl trnsfer from other nimls (wild or domestic), nd contminted feed nd wter. There is cler evidence tht coloniztion of confined poultry flocks cn lso result from the entrnce of Cmpylobcter from the immedite externl environment (which my originte from nerby wstes or from wild vins), s demonstrted in study of Cmpylobcter-free broiler flocks, housed in snitized fcilities, using stndrd biosecurity mesures, nd fed Cmpylobcter-free feed nd wter. Seven out of 10 flocks becme colonized with Cmpylobcter by the time of slughter nd two flocks were colonized by Cmpylobcter strins geneticlly indistinguishble from strins isolted from puddles outside of the fcility prior to flock plcement. 62 Although the route of entry ws not determined, this study showed the cpcity for microbes to enter broiler fcilities. Once poultry flock is colonized with Cmpylobcter, the food, wter, nd ir within the house quickly becomes contminted with the bcterium. 62 Contminted ir exiting the house vi ventiltion systems is then potentil source of Cmpylobcter to the externl environment. Cmpylobcter strins with identicl DNA fingerprints to those colonizing broilers hve been mesured in ir up to 30m downwind from broiler fcilities housing colonized flocks. 62 Other pthogens originting in confined niml houses hve lso been identified in the ir downwind from fcilities nd in ir nd groundwter ner IFAP houses. 36,63 66 Dt from n investigtion by the Cndin Food Inspection Agency following n H7N3 outbrek suggest tht in the event of n HPAI outbrek within flock, the virus lod is such tht biocontinment is nerly impossible nd tht virus trnsfers to the externl environment vi the ventiltion system my present exposure risks to nerby poultry houses s well s humn communities. 36 There re dditionl mechnisms by which Cmpylobcter nd other microbes enter nd leve biosecure poultry houses. For exmple, insects my crry microbes in nd out of fcilities through ventiltion systems nd smll openings. This ws demonstrted in study in Denmrk, which found tht Cmpylobcter crrige ws common mong flies surrounding the broiler fcilities, nd tht s mny s 30,000 flies my enter broiler fcility during single flock rottion in the summer months. 67 Additionlly, reserch conducted during n HPAI outbrek in Kyoto, Jpn, in 2004 found tht flies cught in proximity to broiler fcilities where the outbrek took plce crried the sme strins of H5N1 influenz virus s found in chickens of n infected poultry frm. 68 Further, flies serving s potentil mechnicl trnsmitters of HPAI from poultry houses to soils nd wter my pose risk in those regions where intensive poultry production tkes plce within flywys of migrtory wild birds. Rts hve lso been suspected of crrying H5N1 from wild birds to domesticted poultry in Jpn during n outbrek in Together, these observtions suggest tht veterinry nd public helth officils should consider the potentil for non-vin species to crry vin influenz virus from the feces of wterfowl into poultry fcilities s well s from infected poultry flocks into the surrounding environment. Evidence for incresed risks of virus exposure for frmers nd frm workers We hve outlined severl opportunities for pthogen exposures in CAFOs vi occuptionl nd environmentl pthwys. As indicted previously, there re studies demonstrting incresed risks of bcteril infections mong frmers nd frm workers. A number of studies lso demonstrte tht zoonotic viruses cn be trnsmitted cross the niml-humn interfce in the context of food niml production (Tble 2). Studies on seroprevlence of H1 swine influenz virus infections 27,70 nd heptitis E 22 indicte tht frmers nd frm workers cn be infected by viruses from food nimls. Myers et l. reported tht swine frmers hd higher titers of H1N1 nd H1N2 ntibodies nd gretly elevted risks of seropositivity to these two influenz A viruses (35.3 nd 13.8 odds rtios, respectively, s compred with community referents). 70 There re lso severl studies of recent outbreks of vin influenz in which poultry workers hve been

10 Infectious Disese in Industril Food Animl Production 291 Tble 2. Results of recent studies of zoonotic influenz infection mong frm workers Study Virl subtype Results Cross-sectionl survey of H1N1 (swine) Odds rtio of presence of virl ntibodies by job ctegory 111 Iow swine workers nd (compred with community referents) 79 community referents 35.5 (frmers) 17.8 (veterinrins) 6.5 (metpckers) H1N2 (swine) 13.8 (frmers) 9.5 (veterinrins) 2.7 (metpckers) Cross-sectionl study of H7N7 (vin) Prevlence of virl ntibodies by job ctegory (percent): 453 poultry workers in The 41.0 (cullers) Netherlnds reporting flulike 26.4 (veterinrins) symptoms b 14.7 (frmers nd fmily members) Cross-sectionl study of H5N1 (vin) Prevlence of virl ntibodies by job tsks (percent): 1,525 poultry workers nd 5.8 (touching live poultry) 293 government controls in 3.1 (butchering live poultry) Hong Kong c 2.4 (feeding live poultry) 1.2 (clening poultry stlls) Cross-sectionl study of 74 H1N1 (swine) Risk fctors ssocited with seropositivity to swine influenz swine frm workers nd 114 (H1 titers.1:80). urbn controls in Wisconsin d Being frm owner Being frm owner or fmily member of frm owner Living on swine frm Entering swine brn more thn 4 times/week Age.50 yers Myers KP, Olsen CW, Setterquist SF, Cpuno AW, Donhm KJ, Thcker EL, et l. Are swine workers in the United Sttes t incresed risk of infection with zoonotic influenz virus? Clin Infect Dis 2006;42: b Koopmns M, Wilbrink B, Conyn M, Ntrop G, vn der Nt H, Vennem H, et l. Trnsmission of H7N7 vin influenz A virus to humn beings during lrge outbrek in commercil poultry frms in the Netherlnds. Lncet 2004;363: c Bridges CB, Lim W, Hu-Primmer J, Sims L, Fukud K, Mk KH, et l. Risk of influenz A (H5N1) infection mong poultry workers, Hong Kong, J Infect Dis 2002;185: d Olsen CW, Brmmer L, Esterdy BC, Arden N, Bely E, Bker I, et l. Serologic evidence of H1 swine influenz virus infection in swine frm residents nd employees. Emerg Infect Dis 2002;8: studied. Two smll studies in Itly nd Cnd reported on exposure of poultry workers to H7 HPAI viruses. 1,71 More comprehensive studies hve been conducted in Hong Kong nd the Netherlnds. In study of exposures to H5N1 during the Hong Kong outbrek in , 1,525 poultry workers nd 293 government workers involved in outbrek investigtions were ssessed for risk fctors for seropositivity. 72 Only those occuptionl tsks involving contct with live poultry were ssocited with incresed risks of seropositivity; s shown in Figure 5, the percentge of people with H5 ntibodies rose with incresed numbers of such occuptionl contcts. A study of H7N7 infection mong people reporting relevnt symptoms ws conducted during lrge outbrek of vin influenz in the Netherlnds in At the time of the outbrek in Februry 2003, ll poultry workers, frmers, nd their fmilies were sked to report symptoms of conjunctivitis nd flulike illness to the helth deprtment. Among 453 people clling into the helth deprtment from the region of the outbrek, H7 virus ws detected from swbs in 86 people, in 26.4% of those with conjunctivitis nd in 9.4% of those with conjunctivitis nd flulike symptoms. The highest frequencies were observed in cullers (41.2%), veterinrins (26.3%), nd frmers nd their fmily members (14.7%). In second phse, ll those in close contct with people confirmed to crry H7 were lso sked to enroll in the study. Three of the 83 people contcted in this mnner were confirmed to hve H7 virus s well. All of them were fmily members of frmers. Evidence for incresed risks of HPAI in confined poultry flocks We hve tested the hypothesis tht confined poultry opertions my present incresed risks of HPAI through n nlysis of dt provided by Tiensin et l. 74,75 on the

11 292 Prctice Articles 2004 HPAI epidemic in Thilnd, which lso includes seprte dtset from the ntionwide ctive surveillnce progrm undertken by the Thi government to detect HPAI infections in poultry. These dt re unique nd highly relevnt to ddressing questions on biosecurity nd biocontinment risks ssocited with different modes of poultry production. In the originl 2005 report, Tiensin et l. clssified flocks s bckyrd or commercil nd clssified the poultry by species: duck, geese, quil, lyer chickens, or broiler chickens. 75 Most of the poultry popultion in Thilnd t the time consisted of broiler chickens kept by commercil enterprises, while bckyrd opertions mde up most of the flocks (Figures 6 nd 7). Bckyrd flocks, which consist of 30 birds per flock on verge, constituted pproximtely three-qurters of flocks but ccounted for only bout one-fifth of the totl poultry popultion. Commercil broiler enterprises, consisting of 3,500 birds per flock on verge, constitute only 2% of ll flocks but ccount for nerly 60% of the totl poultry popultion. The Thi poultry industry is lso regionlly concentrted, with commercil production being prticulrly importnt in the Centrl nd Estern regions (Figure 8). In contrst, production of ducks nd geese in the North, Northest, nd South re minly bckyrd opertions. 75 The mjority of quil lso pper to be commercilly rised, s the verge flock size in the Centrl region ws 9,000 birds. A totl of 1,769 flocks with HPAI infection were reported to or detected by the Thi niml helth uthorities in The distribution of these infections by flock type indictes tht more thn 50% of the registered infections involved bckyrd flocks. However, the proportionl contribution of different flock types to registered infections (number of flocks ffected by HPAI) ws mrkedly different from their contribution to the totl number of flocks. The crude risk of detected infection, expressed s percentge of the flock type, is shown in Figure 9. Thus, for exmple, lthough lyer flocks only constituted 1% of ll flocks, they ccounted for 5% of ll registered infected flocks. Quil flocks showed the highest risk of infection roughly 1.6% followed by lyer nd broiler flocks, both with infection risks of just bove 0.2%. Aginst expecttions, bckyrd flocks showed the lowest risk of infection with HPAI (0.05%), only one-qurter tht of lyer nd broiler flocks. These results could reflect differences in outbrek scertinment. It is likely tht HPAI is more redily detectble by the personnel in lrge commercil opertions nd more likely to be brought to the ttention of niml helth uthorities. It is not possible to determine the ctul impct of underreporting in these dt. Figure 5. Percentge of poultry workers seropositive for H5 ntibody by number of poultry-relted tsks performed Bridges CB, Lim W, Hu-Primmer J, Sims L, Fukud K, Mk KH, et l. Risk of influenz A (H5N1) infection mong poultry workers, Hong Kong, J Infect Dis 2002;185:

12 Infectious Disese in Industril Food Animl Production 293 Figure 6. Contribution of different flock types to totl domestic poultry popultion (pproximtely 280 million birds) in Thilnd in 2004 Tiensin T, Chitweesub P, Songserm T, Chisingh A, Hoonsuwn W, Burnthi C, et l. Highly pthogenic vin influenz H5N1, Thilnd, Emerg Infect Dis 2005;11: However, given the focus on bckyrd opertions nd the ctive surveillnce progrms tht were in plce in Thilnd t this time, this potentil scertinment bis is unlikely to be the sole explntion for the higher risk of identified HPAI outbreks in commercil lyer nd broiler flocks compred with bckyrd opertions. Another explntion for these differences my be due to other risk fctors relted to HPAI, such s ecologicl nd regionl fctors, which might modulte Figure 7. Contribution of different flock types to totl number of flocks (pproximtely 2.9 million flocks) in Thilnd in 2004 Tiensin T, Chitweesub P, Songserm T, Chisingh A, Hoonsuwn W, Burnthi C, et l. Highly pthogenic vin influenz H5N1, Thilnd, Emerg Infect Dis 2005;11: trnsfers from wild vins nd mong domesticted flocks. From temporl nd geogrphicl perspective, HPAI outbreks in Thilnd in 2004 were shown to be linked to certin gro-ecologicl fctors, such s the geogrphicl density of wetlnds nd rice pddies. 76 The Centrl region ws prticulrly ffected, followed by the Estern region, while the Northern, Northestern, nd Southern regions only experienced minor epidemics. 75 Given tht these different regions lso hve different mixtures of flock types, the dt were subjected to sttisticl multivrite nlysis to control for potentil confounding mong region, flock typespecific risks, nd verge flock size within region nd species ctegory. Logistic regression nlysis ws used with vrible selection being bsed on the likelihood rtio sttistic. Additionlly, the Huber-Sndwich estimtor ws used to obtin djusted coefficient estimtes due to clustered dt. Tble 3 displys the djusted odds rtios (nd their 95% confidence intervls) for the selected risk fctors, tking bckyrd opertions nd the Northestern region (lowest crude risk) s reference groups (odds rtio = 1). The multivrite sttisticl nlysis shows tht there ws n interction between region nd species, such tht within the North nd Centrl regions, mong the flock types in the region, bckyrd flocks hd the lowest odds rtios of outbrek occurrence. In the Est, there ws reltively little difference between flock types, but lyers nd geese hd the highest odds rtios. In the South, the odds rtios of infection were not different from bckyrd flocks in the Northest for lyers, ducks, nd quil, but they were higher for bckyrd nd broiler flocks. In the Northest, lyers nd quil hd higher odds rtios thn bckyrd flocks, wheres they were reduced in ducks, lyers, broilers, nd geese in the South nd Northest. Across regions, the odds rtios for quil flocks to experience HPAI infection were by fr the highest. Overll, these results reflect the geogrphicl pttern of the outbreks, most of which occurred in the centrl region of the country, nd the lowest number in the South. In 2004, the Thi government implemented two dditionl progrms designed to improve erly detection of vin influenz infections in poultry. One of these, preemptive culling, involved responses bsed on elevted mortlity in flock, nd the other involved n ctive ntionwide surveillnce progrm to detect possible HPAI infections in the bsence of incresed mortlity. In this ltter progrm, swb smples were tested by severl methods, including ntibody mesurement nd rel-time polymerse chin rection. 74,75 These dt indicte higher numbers of detections in birds from bckyrd flocks s opposed to those from

13 294 Prctice Articles Figure 8. Sptil distribution of poultry popultion counts t district level in Thilnd in 2003

14 Infectious Disese in Industril Food Animl Production 295 Figure 9. Risk of infection (percent) with HPAI in Thilnd in 2004 by flock type HPAI 5 highly pthogenic vin influenz commercil broiler flocks; however, bsed upon the design, there ws progrmmtic focus on bckyrd flocks tht resulted in oversmpling of bckyrd flocks reltive to commercil flocks. We do not hve the dt to exmine this possibility. In the ctive surveillnce progrm, clocl swbs were rndomly collected from five birds per flock nd four flocks per villge. Over the period of surveillnce, swbs were collected from pproximtely 230,000 flocks in more thn 50,000 villges. As indicted previously, for our nlysis of outbrek dt, on flock bsis, compred with commercil flocks lrger number of bckyrd flocks my hve tested positive, but within these infected flocks much lrger numbers of infected nimls will hve been present in commercil thn in bckyrd flocks. This mens tht commercil flocks once infected represent formidble chllenge for biocontinment of the infection. This issue includes the problem ssocited with the disposl of ded birds following culling s prt of control effort. Tken together, the dt do not support the ssumption tht bckyrd poultry production in Thilnd presents more of risk, in terms of HPAI outbreks, thn lrger commercil poultry opertions (either ly- ers, broiler chickens, or quil). There re no dt tht permit exmintion of other production fctors, prt from flock type nd species, which might prticulrly contribute to incresing or decresing HPAI infection risks within nd between flock types. Similrly, dt from Cnd, lthough incomplete, hve lso indicted tht in contrst to bckyrd flocks, lrge commercil opertions were disproportiontely ffected by 2004 HPAI outbrek. 36 CONCLUSIONS Understnding the niml-humn interfce is criticl element in evluting nd predicting risks of emergent zoonoses, s well s in designing evidence-bsed progrms for prevention nd erly detection of emerging infectious diseses, such s vin influenz. This hs been well documented in terms of zoonoses rising from wild niml species 77 nd in regrd to food sfety, 78 but it remins underrecognized in terms of workers involved in the production of domesticted nimls. There hve been mjor chnges in mny spects of domestic food niml production in the U.S. nd other countries during the 20th century, resulting in

15 296 Prctice Articles industril-scle opertions involving high densities of confined niml popultions, which is how most of the world s niml protein sources re now derived. These chnges in orgniztion, intensity, housing, nd wste genertion my influence the emergence nd trnsfers of vin influenz virus mong wild nd domestic species, nd from vins to humn popultions. If this is the cse, then inferences bsed upon the lst globl nd ntionl experience with pndemic vin influenz in my need reconsidertion. Most importntly, the modern methods of both poultry (prticulrly broiler chickens) nd swine production hve chnged. These opertions result in high numbers of poultry nd swine housed under confined conditions t gret density nd geogrphic concentrtion. These opertions hve lso chnged the mngement nd utonomy of niml husbndry: individul frmers re incresingly supplnted by lrge producers tht contrct with growers to rise nimls. Tble 3. Adjusted odds rtio (OR) nd 95% confidence intervl (CI) for selected risk fctors for HPAI infection in Thilnd in 2004 Region Flock type OR 95% CI Northest Bckyrd 1.0 Lyers , 11.5 Broilers , 4.4 Ducks , 0.6 Quil , Geese , 11.2 North Bckyrd , 13.5 Lyers , Broilers , Ducks , 23.3 Quil 1, , 1,986.1 Geese , 79.2 Centrl Bckyrd , 31.1 Lyers , Broilers , Ducks , Quil 1, , 1,636.2 Geese , Est Bckyrd , 20.7 Lyers , 74.9 Broilers , 30.3 Ducks , 29.4 Quil Geese , South Bckyrd , 2.3 Lyers , 11.2 Broilers , 18.4 Ducks , 2.2 Quil , 47.8 Geese HPAI 5 highly pthogenic vin influenz This hs implictions for public helth surveillnce nd interventions, s the frmer no longer mkes decisions in reltion to feeding, housing, or opertions. Access to niml fcilities is lso incresingly controlled by producers rther thn frmers. These chnges in some cses my hve beneficil impcts in terms of erly detection nd veterinry oversight. These new methods of food niml production generte mny routes of pthogen trnsfer mong wild nd domesticted species nd from nimls to humns through occuptionl, peri-occuptionl, nd environmentl pthwys. At the niml-humn interfce in these opertions, there is indequte protection of workers nd their communities, nd, more generlly, there is incomplete biocontinment to prevent trnsfers from the niml house to the generl environment. Indeed, the min emphsis of disese prevention with incresing production intensity is typiclly on enhncing biosecurity, wheres biocontinment is considered less of priority. Evidence would suggest tht once pthogen hs been introduced into such production fcility, it cn rpidly multiply; for some pthogens, enormous quntities of infectious orgnisms cn be relesed nd expose other production units. For exmple, it hs not been recognized tht the necessity for high ventiltion of densely confined nimls gretly impirs ttempts t biocontinment. Moreover, little ttention hs been given to the genertion nd lck of mngement of the millions of tons of niml wstes generted nnully. Food niml wstes re lrgely disposed on lnd, nd this cretes n unrecognized mgnet for wild vins becuse of the presence of undigested feed in the wste. There is some use of poultry wstes s bedding for fish ponds, which cretes n dditionl opportunity for wild vin contct. Studies of bcteril pthogens provide strong evidence for the bidirectionl trnsfers of pthogens mong poultry grown in these confined opertions, wild birds, nd humn popultions. Our nlysis of the Thi HPAI outbrek nd surveillnce dt suggests tht commercil poultry production, n ostensibly more biosecure system of production, is not ssocited with reduction in risk of HPAI infection t the frm or flock level, s compred with tht experienced by subsistence bckyrd producers. Although the mjority of reported HPAI outbreks in Thilnd in 2004 occurred in the ltter, this incresed cumultive risk of HPAI in the bckyrd sector is primrily due to their reltively greter numbers rther thn more risky production prctices. Some of the mesures being considered to mke bckyrd poultry production sfer, including the forced housing or confinement of poultry, re not likely to

16 Infectious Disese in Industril Food Animl Production 297 result in mjor reduction of HPAI risks. In contrst, the costs will likely be significnt nd will be imposed upon mrginl group of entrepreneurs nd household producers. This my result in n overll reduction of HPAI outbreks s consequence of the loss of household production flocks, but not s result of enhnced biosecurity nd biocontinment. Additionlly, the geogrphic concentrtion nd housing density of commercil poultry production cn gretly ugment the spred of HPAI in n infected re. A study of n outbrek in The Netherlnds found tht the trnsmission rte of the virus ws not necessrily ffected by improved biosecurity nd biocontinment mesures but by depletion of susceptible flocks due to complete depopultion of infected res. 79 The uthors suggested tht reducing flock density in commercil flocks might reduce the probbility of mjor epidemic in which lrge numbers of poultry flocks must be culled. Following the forementioned HPAI outbrek in Cnd, restriction permits for the development of new opertions were proposed s method to control the density of commercil opertions when deemed too close to existing frms. 36 This nlysis suggests tht renewed ttention to the niml-humn interfce should focus on high-risk popultions, especilly frm workers. A similr conclusion ws reched by Senz et l. 18,80 in n nlysis of the risks of influenz outbreks nd trnsmission to humn popultions in the context of lrge-scle commercil poultry nd swine production. Monitoring this popultion my improve detection of erly events in emergence of vin influenz. In ddition, creful evlution of opertions t ll poultry fcilities lrge nd smll should be undertken to reduce opportunities for the trnsmission of disese mong vin nd other species. Moreover, if pproprite protections such s vccintion re identified, the griculturl workforce constitutes high-risk popultion for whom protection from zoonotic disese is importnt not only for their helth but for the helth of their communities nd the popultion t lrge. Finlly, improved oversight nd mngement of niml wstes including trnsport nd sle s well s use in quculture should be included in strtegies to reduce risks of pndemic HPAI. The uthors re grteful for support from the Center for Livble Future t the Johns Hopkins Bloomberg School of Public Helth. The uthors lso thnk Slvdor Senz from the Center for Environmentl Resource Mngement t the University of Texs t El Pso for his wonderful rtwork; Dr. Ruth Fden nd Ruth Krron of the Johns Hopkins Medicl Institutions for providing the opportunity for this collbortion; nd Dr. Pierre Gerber from the Food nd Agriculture Orgniztion of the United Ntions. 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