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TECHNICAL REPORTS

1086

A are ued amal lvek prdu frherapeu reame f deae ad a uherapeu levelfr grwh prm ad mprveme f feed effi ey.I emaed ha apprxmaely 75% f a are ared y amal ad are exreed wae. A

reae ele ur amg gareal aera,whh are al exreed maure ad red wae hldgyem. Lad appla f amal wae a mmdpal mehd ued he Ued Sae ad a mea frevrmeal ery f h a ad gee reaedeerma. Cer fr aeral reae gee elead dema f reae gee have prmped ereau he era ad lgal avy f drug reduead reak-dw meale, ad her fae ad rapr. Fealaera a urvve fr week mh he evrme,depedg pee ad emperaure, hwever, geeeleme a per regardle f ell valy. Phylgeeaalye dae a reae gee have evlved,alhugh me gee have ee maaed aera efrehe mder a era. Quaave meaureme f drug

redue ad level f reae gee are eeded, add uderadg he evrmeal meham f geeele, gee aqu, ad he paempral dyamf hee reae gee ad her aeral h. T revewarle due a aumula f fidg ha addreape f he fae, rapr, ad peree f aad a reae gee aural evrme, whempha meham perag l evrmefllwg lad appla f amal wae effl ue.

Fate and Transport of Antibiotic Residues and Antibiotic Resistance Genes

following Land Application of Manure Waste

Joanne C. Chee-Sanford* USDA-ARS, University of Illinois

Roderick I. Mackie and Satoshi Koike University of Illinois

Ivan G. Krapac Illinois State Geological Survey

Yu-Feng Lin Illinois State Water Survey

Anthony C. Yannarell and Scott Maxwell University of Illinois

Rustam I. Aminov Rowett Research Institute

Antibiotics are ruely ued he lvek dury rea ad preve deae. I add, uherapeuera f amral are mmly added amalfeed ad/r drkg waer ure a grwh prmer, ad

have ee a regular par f we (Sus scrofa) prdu ehe early 1950 (Crmwell, 2001). Whe ued h maer,a a ele fr rea aera he garealra f prdu amal, prvdg a peal reervr frdema f drug rea aera her amal,huma, ad he evrme (Adrem, 2003). Baerahave ee hw readly exhage gee frma aure, permg he rafer f dffere reae mehamalready pree he evrme frm e aerum aher (Salyer ad Amle-Cueva, 1997; Amle-Cueva adChurel, 1992; Sewar, 1989). rafer f reae gee frmfeal rgam dgeu l ad waer aera may ur(Nele e al., 2000; Daae e al., 1996; DGva e al., 1996;Lrez ad Wakeragel, 1994), ad eaue ave ppulaare geerally eer adaped fr urvval aqua r erreraleyem, peree f reae ra may e lkely auralevrme e hey are aqured. A reae hareeved derale ae due he prlem f emergeead rapd expa f a rea pahge aera.

Te peal fr lg-erm, umulave pu f a adrrepdgly, her peal effe aqu ad mae-ae f a reae meham aera, llevely ug-ge a degree f mpa he urree, peree, ad mly

Abbreviations: CAFOs, concentrated animal eeding operations; MICs, minimum

inhiabitory concentrations; OTC, oxytetracycline; PCR, polymerase chain reaction;

RPPs, ribosomal protection proteins; SCP, sulachlorpyridazine; UCS, Union o

Concerned Scientists.

J.C. Chee-Sanord, USDA-ARS, 1102 S. Goodwin Ave., Urbana, IL 61801, and Dep. o

Crop Sciences, Univ. o Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801; R.I. Mackie, S.

Koike, and A.C. Yannarell, Dep. o Animal Sciences, and Division o Nutritional Sciences,Univ. o Illinois, 1207 W. Gregory, Urbana, IL 61801; R.I. Mackie, Institute or Genomic

Biology, Univ. o Illinois, 1206 W. Gregory, Urbana, IL 61801; I.G. Krapac, Illinois State

Geological Survey, 1910 Grif th Dr., Champaign, IL 61820; Y.-F. Lin, Ill inois State Water

Survey, 2204 Grif th, Champaign, IL 61820; S. Maxwell , Dep. o Natural Resources and

Environmental Sciences, Univ. o Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801; R.I.

Aminov, Rowett Research Institute, Greenburn Rd., Bucksburn, Aberdeen AB21 9SB,

Scotland, UK.

Copyright 2009 by the American Society o Agronomy, Crop Science

Society o America, and Soil Science Society o America. All rights

reserved. No part o this periodical may be reproduced or transmitted

in any orm or by any means, electronic or mechanical, including pho-

tocopying, recording, or any inormation storage and retrieval system,

without permission in writing rom the publisher.

Published in J. Environ. Qual. 38:10861108 (2009).

doi:10.2134/jeq2008.0128

Received 14 Mar. 2008.

*Corresponding author ([email protected]).

ASA, CSSA, SSSA

677 S. Segoe Rd., Madison, WI 53711 USA

REVIEWS AND ANALYSES

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1088 Journal o Environmental Quality Volume 38 MayJune 2009

marly hrugh amma vlalza ad a N2

r N2O gae

(Harper e al., 2004; Rz, 2004). Te l f N ad he eque-erg f muh f he P wae lag ludge a redue heamu f lad requred fr wae dpal mee agrm

gudele fr e maageme prae (Beegle, 1997).Te m mm mehd dpe f we ad feedl

ale wae effl ue he Ued Sae fllwg lag r prage hrugh lad appla, where appla f lqudmaure a agrm rae a prdue rp yeld ha equalhe aed wh hemal ferlzer (Shm e al., 1995;Sarmah e al., 2006). ue ad dpe f he maure effl u-e, CAFO perar fe ra wh eghrg grwer apply effl ue her lad r apply lad urrudg he

faly. Beaue ly rapr lqud effl ue ay greadae, here a eve apply effl ue a le heure a ple. I he Ued Sae he rp yle dewh eaal yle, wh he appla f maure urrgewee rp yle. Fr may la, maure red fr6 m 1 yr efre eg appled rp field a ferlzer. Ef-flue dffer frm freh maure ha ha a muh greaer

Fig. 1. Conceptualized view showing the possible ates o antibiotic residues and mechanisms o antibiotic resistance gene acquisition anddissemination by bacteria, beginning with land application o animal waste as the source o entry o drugs, bacteria, and resistance genesinto the soil environment. AB = antibiotic, ABR = antibiotic resistance.

Table 1. Survey o the most commonly used antibiotics in animalproduction (AHI, 2001).

Antibiotic class Amount

metric tonnes

Ionophores/Arsenicals 3520

Tetracyclines 3239

Other antibiotics-includes macrolides, lincosamides,polypeptides, streptogramins, cephalosporins

1937

Penicillins 821

Sulonamides 269

Aminoglycosides 117

Fluoroquinolones 16

Table 2. Antibiotics commonly used in swine, poultry, and bee cattleproduction industries (USGAO, 1999; USDA, 2007).

Antibiotic class Industry

Aminoglycosides Swine, poultry, bee cattle

-Lactams Swine, poultry, bee cattle

Chloramphenicol Bee cattle

Ionophores Poultry, bee cattle

Lincosamides Swine, poultry

Macrolides Swine, poultry, bee cattle

Polypeptides Swine, poultry

Quinolones (and Fluoroquiniolones) Poultry, bee cattle

Streptogramins Swine, poultry, bee cattle

Sulonamides Swine, poultry, bee cattle

Tetracyclines Swine, poultry, bee cattle

Others:

Glycolipids (Bambermycin) Swine, poultry, bee cattle

Carbadox Swine

Aminocoumarins (Novobiocin) Poultry

Aminocyclitols (Spectinomycin) Swine, poultr y

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Chee-Sanord et al.: Fate & Transport o Antibiotic Residues & Antibiotic Resistance Genes 1089

waer vlume. Freh we wae a apprxmaely 10%ld, whle deep p ad lag effl ue are 4 8% ld ad

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relavely hydrph (ll, 2001). Addally, he wa-er luly fr may a exeed 1 g/L uggeg hahey are relavely hydrphl (ale 3). ll (2001) ad Bx-all e al. (2004) mpled rp effi e (K

d) fr a varey

f a, l, ad l mpe meaured ver he

ure f may ude. Baed Kd value, a exha rage f affi e fr he ld phae (K

d0.26000 L/kg) wh

eque effe her mly he evrme. E-ma f a rga ar-rmalzed rp ef-fie (K

) made y ug a mpud al-waer par-

effi e (Kw

) geerally reul uderemae f heK

value, uggeg ha meham her ha hydrph

parg ur. Ca exhage, urfae mplexa,ad hydrge dg are luded a lkely meham fra rp l. May f he ad da -a (pK

a) fr a are he rage f l pH value,

uh ha he pra ae f hee mpud deped

he pH f he l lu (ll, 2001).Sude have hw ha uder a rad rage f evr-meal d, erayle (erayle, hlreray-le, ad xyerayle) a adr rgly lay (Al-lare e al., 2006; Shle ad Guy, 1987a, 1987; Pk eal., 1961a,1961), l (Krapa e al., 2004), ad edme(Ralle ad Spld, 2000). Srp f hlrerayle alurred rapdly ady lam l (Allare e al., 2006). Ma-rlde uh a yl have a weaker edey r lmaeral (Ralle ad Spld 2000), hwever a rp ke

udy hwed 95% f yl wa red wh 3 h hady lam ad lay l (Allare e al., 2006). Sulfamdeexh weak rp l, ad lkely are he m mle fhe a (ll, 2001). Pk e al. (1962) deermedha w marlde a (army ad eryhrmy-

) red gfialy (231263 mg/g) mmrllead a muh leer exe (039 mg/g) vermule, lle,ad kale. I a leraure revew he fae f a he evrme Huag e al. (2001) luded ha herewa lle frma he rp f amglyde ad-laam a. Beaue amglyde a e pr-aed uder ad d, hey uld e red laymeral uder era d, whle -laam are hghlyplar mpud ad wuld e expeed r readly l mpe. Beaue f he rg rp f he e-rayle ad marlde a, her mly he ev-rme may e falaed y rapr wh maure ad l

lldal maeral (Klz e al., 2005a). Ieregly, alhughm a d requre meal rda exerlgal a, her mpud lke ara, rep-gr, lemy, ad erayle have prereque fr d-g f meal fu prperly (Mg, 2003). Srpf hee drug mpud lay, where erala f mealmplexe ur, may prvde uale d fr he drug exer a lgal effe.

Table 3. Chemical properties and ate o selected veterinary antibiotics (modifed rom Beausse, 2004; Boxall et al., 2004; Tolls, 2001).

Antibiotic Solubility in water Log K ow

Log Koc

Kd

pKa

and chemical degradation Mobility

g/L L/kg

Lincomycin(hydrochloride salt)

reely ND ND ND pK a

7.6In spiked soil 10 mg/kg undetectable ater11 wk and 80% lost ater 7 wk

Immobile especially in highorganic matter/clay soilbased on manuacturercolumn tests.

Sulathiazole 0.6 0.05 2.30 4.9 pK a1

2, pKa2

7.24 Medium mobility based

on KdSulamethazine 1.5 0.89 1.782.32 0.63.1 pK

a12.65, pK

a27.65

Biodegradable but persistent in water phaseHigh to medium basedon K

d

Tylosin 5 3.5 2.743.90 8.3240 pK a

7.1Stable at pH 4 to 9, < pH 4 desmycosin isormed.

Low to immobile basedon K

d

Virginiamycin 0.054 0.080 1.51.7 2.72.8 ND T1/2

: 87173 d89% inactivated within 18 d andundetectable ater 84 d.Activity decreases rapidly in water andincreasing temperature. Degrades underalkaline pH.

Immobile due to low watersolubility, high lipophilicityand rapid inactivation insoil.

Tetracycline 1.7 1.19 ND >4001620 pK a1

-3.30, pKa2

-7.68, pKa3

-9.69 Immobile based on K d

Chlortetracycline 0.6 0.62 ND 2822608 T1/2

in manure 1 wk at 37C & > 20 d at 4or 28C85% o CTC added to soil was recovered.

Immobile based on Kd

Oxytetracycline 1 1.22 1.25.0 0.31030 pK a1

3.27, pKa2

7.32, pKa3

9.11Stable compared to CTC

Immobile based on Kd

Ciprooxacin 30 0.4 4.78 430 pK a1

5.9, pKa2

8.89 Immobile based on K d

Enrooxacin 130 1.1 4.225.89 2606310 pK a1

6.27, pKa2

8.3 Immobile based on K d

Penicillin 4 1.87 ND ND pK a

2.79Unstable, rapidly degrades to penicilloicacid. T

1/2< 7 d

Weakly sorbed to soils

ND = not determined or not ound in the literature reviewed.

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Mechanisms of Antibiotic Degradation

Beaue a are geerally rdued frm lvekpera va waer (effl ue) he evrme, hydr-ly a e a mpra degrada pahway. Bea-laam,marlde, ad ulfamde appear e he m ueplelae f a hydrly (Huag e al., 2001). A eareural pH, yl A wa fud have a hydrly half-lfe f300 500 h a 60C (Paee e al., 1995). A mre evr-meally releva emperaure, hee half-lve are expeed e lger. D ad Skpf (2000) deermed ha uder rela-vely hgh emperaure (43C) he half-lfe f xyerayle dezed waer wa 0.26 d, u wa relavely ale a 4C.Bea-laam are rapdly hydrlyzed uder mld ad ad ad (Huag e al., 2001; Hu ad Ple, 1969).

Phly a e aher a rafrma pre af-feg a rdued he evrme. Te ph-degrada f a l a ur a he l-am-phere erfae ad a he urfae f lqud maure. Sl aprvde a muh dffere phdegrada evrme haaqueu lu ad rafrma rae a vary gfialy

l mpared he waer (Balmer e al., 2000). Qu-le ad erayle are ueple phdegrada(Huag e al., 2001), ad phdegrada f xyerayle wa hree me mre rapd uder lgh ha dark d(D ad Skpf, 2000). Hallg-Sree (1998) uggeedha yl mgh e rea phly eaue ha lylmed lgh arae he vle perum, ad Bxall eal. (2004) deermed ha ulfamde wuld e readlyphdegraded. Beaue (2004) luded ha phdemp- f a uder field d were eglgle whempared wh her a pree.

Lmed umer f ude ae he degrada fa have ee dued. Depedg e d,

degrada half-lve f rga mpud a wdely vary.Sude ug adard larary e aay have demraedlmed r degrada f a uh a merdazlead xyerayle (Kmmerer e al., 2000; Samuele e al.,1994; Jae ad Bergld, 1988). I aher udy f 18 a- eed, e were fud readly degraded (027% fhe pare mpud l) afer 28 d, ad me ae ur-rg ly whe addal ure uppleme wa made (Alexye al., 2004). Pell G wa fud readly degradale algwh me degrada f amxll, mpeem, ad ya- (Garer e al., 2007a, 2007). A udy f aquaulure ed-me hwed aeral meralza f eryhrmy A (Kme al., 2004). Ihere he pre f degrada, he x

effe f a he rede aera have al ee dem-raed. A rage f a era were fud h avaed ludge wae waer reame (Garer e al.,2007a; Alexy e al., 2004), hwever ye ukw he exaeffe f a ery aural evrme mralppula rede hee yem.

Pla upake ad aumula f a ha reevedderale ere due ue f fd afey ad humahealh. A umer f ude have hw h meham -

ur wh a varey f pla pee (e.g., Dllver e al., 2007;Bxall e al., 2006; Kumar e al., 2005), ad furher luderafrma f mpud hrugh well-kw pla de-xfia meham (Park ad Chug, 2007; Saderma,1992). Whle gfia he fae f a, du fhee pree ude f he pe f h revew.

Persistence of Antibiotics in Manure

A exreed frm amal are fe eraed he ld phae eaue f rp dyam (Klz e al., 2005a,2005; Lke e al., 2002; ll, 2001). Half-lve ha have eerepred fr a varey f a lae maure (Bxall eal., 2004) (ale 4) were le ha he apaed rage perdf maure, uggeg he ply ha gfia degradaf he pare mpud mgh ur efre lad appla.Qule ad erayle were he m pere wh half-lve apprahg 100 d. Klz e al. (2005a) deermed ha90% f yl, yl B, ad yl D ha were added a hear f he experme were deeed he exraale fra- f he lurry mxure wh 30 130 h aaer ma-ure lurre a 22C. Aerag he lurre redued he me

aheve 90% l f yl 12 26 h. Alhugh degrada- ad a degrada urred, he prmary mehamfr yl l wa hugh e rreverle rp ma-ure ld (Klz e al., 2005a, 2005). Redual yl ad reakdw prdu, dhydrdemy, were al deeed he lurre afer 8 m. I everal ude, erayle era- were fud geerally hgher ha marlde, -laam,ad ulfamde (ale 5). erayle era mewe lag were a grea a 1 mg/L (Campagl e al., 2002).Gavalh ad Kaz (1994) deermed he peree f evea a l-fee marx uder larary d adfud ha he rder f peree wa hlrerayle > a-ra > eryhrmy > repmy amermy yl pell wh regard her dee he l. Te ap-pla f maure agrulural field al lkely rduereakdw prdu he evrme alg wh he parempud, hwever, peree daa fr degrada prduwere fud he revewed leraure. Te aure f heereakdw prdu pera he peal lgal avef hee hemal, alg wh he pare mpud. Te lakf frma reakdw meale aural evr-me a large par e arued aalyal dffi ule adaly f upeed r ukw meale (OCr adAga, 2007; Igerlev ad Hallg-Sree, 2001).

Persistence of Antibiotics in Soil and Water

Ul reely, frma regardg he urree, fae,ad rapr f a uder field d ha eelmed. I a ady l ha had repeaed we lqud maureappla, erayle ad hlrerayle were deeeddw a deph f 30 m (Hamher e al., 2002, 2005). Tehghe erayle ad hlrerayle era, 198ad 7.3 g/kg, repevely, were deeed a l deph f 10 20 m ad 20 30 m, repevely. Sulfamehaze wa ge-erally deeed l ample, u wa deeed grud-

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waer lleed a a deph f 1.4 m. Oxyerayle, ulfad-aze, ulfahazle, ulfameraze, ulfamehxypyrdaze,ulfamehxazle, ulfadmehxe, ad yl were de-eed ay l r grudwaer ample. Whle appearedme f he erayle uld aumulae l, e f hea frm he udy were deeed a l deph >30 mad ly ulfamehaze wa deeed grudwaer ugge-g lmed rapr, eve hghly pru ady l.

I a field udy wh lay lam l ha reeved we ma-ure pked wh he ulfamde, ulfahlrpyrdaze (SCP),he a wa fud e mle ad readly eered hefield dra, wh a maxmum era f 590 g/L dee-ed 7 d afer maure appla (Bxall e al., 2002). I he ameudy dued wh ady lam field l, SCP era l pre waer were gfialy lwer (maxmum era- 0.78 g/L) ha he field wh lay lam, ad raedwh larary rp ude ha preded larger l waerera. Te lwer era deeed he fieldample were hyphezed e he reul f SCP degrada.

I aher l rapr udy, SCP ad xyerayle

(OC) were deeed l a era up 365 ad 1691g/kg, repevely (Kay e al., 2004). Smlar her vega-, hee mpud were deeed elw a deph f au37 m. Te SCP ad OC were deeed le draage a peakera f 613 ad 36 g/L, repevely. Oly 0.004% fhe OC ha wa appled wa he parulae phae, ad 23%f OC mved le draage. Te vegar luded hahe a ehaved mlarly pede uder field d-, ad ha le draage may e a gfia rue fr heempud mgrae urfae waer. Te maure h udy

wa urfae-appled whu rpra he l ad heauhr uggeed ha llage efre r durg maure appla- mgh lm rapr f a. I a laer udy y heame auhr, we maure pked wh SCP, OC, ad ylwa urfae-appled whea (Triticum aestivum L.) ule alay lam l ad ma revery f SCP ad OC l urfaeruff wa 0.42 ad 0.07%, repevely (Kay e al., 2005). Whleurfae ruff dd appear e a gfia rapr l,

he auhr uggeed ha rpra f maure he lwuld furher lm l frm he l. yl wa deeed ay ample uggeg rapd degrada he maure,upprg prevu evdee ha marlde may mre readlyuderg mral degrada pree.

I a udy where we maure wa pked wh ulfadazead ulfahaze ad rrgaed gralad,

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agrulural avy flueed erayle urree herver. I a udy dee a urfae- ad grudwaer, Campagl e al. (2002) fud 31 ad 67% f heample lleed ear we ad pulry fieme fale,repevely, had deeale quae f

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may al dereae red effl ue, hwever, h hypheha ye e adequaely eed. Dealed rrela eweeaeral ppula ad her rrepdg a re-ae deerma have ee mprehevely examed.

Tere rg evdee ha hermphl aer r aaer- dge f we maure a rear a redue pah-ge lad y mre ha fur rder f magude (Sey eal., 2001), alhugh he effe f he pre pefially

a-rea aeral ppula, pahge r , geerally ukw. Aaer dge f dffere welurre eh ale equeg ah rear perag aa emperaure f 20C fr 20 d redued he ly frmgu u (CFU/mL) f he al lfrm ppula deeale lm r y 1.62 4.23 lg CFU/mL, ad E.colippula deeale lm r y 2.48 4.16 lgCFU/mL (C e al., 2006). Alhugh lfrm aera frmlvek ypally exh me degree f a reae, ukw wha effe dge reame wuld have he verall a reae f we wae aera.

Persistence of Bacteria Introduced to Soil

Lad appla f amal maure, wh hgh era- f mral ma, a gfia rue fr he rdu- f ew aera he erreral evrme, ludgpeal pahge (e.g., E. coliO157:H7) ad me humaeer vrue (e.g., ravru). Te peree ad rapr fhee rgam he evrme ue e a erfr evrmeal qualy, fd afey, a well a huma ad a-mal healh. Gavalh ad Kaz (1994) luded ha he l-ger a a per he l a ave frm, he greaerhe peal fr ave l aeral ppula e affeed.Nure amedme va he appla f amal wae lha ee hyphezed prme faer adapa f he lmral mmuy a effe (Shm e al., 2005).I add, lgally ave a (r a reak-dw prdu) rdued he l may fer a eleve ad-vaage fr l mmeal aera arryg reae gee, rexer eleve preure fr aqu f reae gee lmmeal ppula.

I ha ee well dumeed ver he year ha may m-rrgam urvve he ra frm effl ue p r lag l (Be e al., 2005; Gua ad Hlley, 2003; Jag eal., 2002; Bl e al., 1999; Lee ad Szky, 1999; Sddarde al., 1998; Chadler e al., 1981; Key e al., 1978). Mvega have hwever, fued pahge f lalere. Te legh f me ha rdued rgam a per-

he l vare wh emperaure, mure, pH, ad hedgeu mmuy pree. Te wde rage f pereeme f fur well-uded pahge dffere evrmead a dffere emperaure ha ee repred (ale 7). Aree udy examg he urvval f E. coliad Salmonellatyphimurium appled a lay l wh we effl ue, hw-ever, fud deraly hrer peree me (21 d fr E.coliad 7 d fr Salmonella typhimurium) (Be e al., 2005),hghlghg he vara urvval me uder dffere e-vrmeal d. Segelv e al. (2003) uded he per-

ee f ulureale aer, heerrph, erayle re-a aera fur Dah farm l fllwg varale raef pg lurry appla. A reae umer f reaaera wa ee fllwg appla, wh greaer rea-e urrg he mre heavly maured l. Fve mhfllwg appla, he prpr f erayle reaaera all f he reaed l had reured level whhe rage f he maured rl ample. Adrew e al.

(2004) fud eer deled frm 4.8 105

CFU/g l

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rapr f aera ha ee a exevely udeda vrue. Vrue a e dered lldal ad may mveuaally faer ha dlved lue, lke rmde, u-urfae evrme a a reul f prefereal flw hrughhe large l aperure ffered y fraure ad r hle. Sl-ue have a hgher praly ha lld f eerg mallerpre, reulg mre ruu, lger, ad ulmaely lwerflw pah. I lay frma, fraure ad r hle a e

a large a 100 m, 5000 me larger ha he malle vrue(Hy e al., 1996), ad vrue a pa hrugh frauredlay ll aperure a mall a 3 5 m (Sm, 1993). M-Kay e al. (1993) hwed ha apprxmaely 50% f lay prehra are maller ha 65 m, whh au he ame zea eer vrue. Te ame udy demraed ha vruePRD-1 ad MS-2 mve hrugh fraured lay a velef 2 5 m/d, whh 100 200 me faer ha rmde.Hy e al. (1996) meaured PRD-1 ad MS-2 vru vel-e f 4 360 m/d hrugh lay wh fraure ad r hle.Depedg edme hemry, vrue may e m-pleely aeuaed y adrp edme gra.

Vrue have ee fud grudwaer a a deph f 67 m

ad are repred mve hrzally a far a 408 m glaalll ad 1600 m fraured lmee (Rer ad Ederg1997; Kewk ad Gera, 1980). Vrue may urvve hlr-a, ulgh, prayg ad perla hrugh ady l(Wellg e al., 1974) ad are apale f urvvg a lea 28d grudwaer (Wellg e al., 1975). Baera ad vrueare wdely avalale fr rapr wh grudwaer yemdue her mm urree drkg waer well (Geraad Re, 1990). Te pree f vral rapr are exremelymplex. A h f majr far a affe uurfae vralrapr, ludg emperaure, mure e, pH, hy-draul d, rga maer, adrp ad derp,al e, ype f vru, vru ava (.e., vru deay),l prpere, rafall, ure f vru ad waer ale deph(Cherry e al., 2007; Azadpur-Keeley e al., 2003; Shjvead Haazadeh, 2000; B ad Harvey, 1992; Yae adYae, 1988; Gera ad B, 1984). Te aly f vrue medae her effe h aera (ad her gee mple-me) hghly depede e-pefi d.

Ae mdelg he rapr f aera, vrue,ad a redue ha are due ere predghe fae ad urree f pahge ad a reaegee. M vru rapr mdel are aed he prmarypree f vral rapr: adve, dper, rp,ad ava (Lvelad e al., 2003) ad are eyd he

pe f du he pree revew. Cmpuer mdelhave ee ued, hwever, ad he ume are hghly he-ergeeu a he field-ale, dffer wdely y vru ype, adare aaed wh a grea deal f ueray (Yae ad Jury1995). Fr example, Yae e al. (2000) mpared prededvru era ug w mdel, CANVAS (Park e al.,1994) ad HYDRUS-2D (Smuek e al., 1999), a epyem leah field. CANVAS pred eher veremaedr uderemaed he field daa. Alhugh HYDRUS-2D a-uraely preded he vru reakhrugh urve, he mdel Ta

ble7.

Persistencetimesopathogenicbacteriaindiferentenvironments.

Estimationosurvivaltime

Environment

Temperature,

C

Salmonella

(Guoetal.,

2002;SantoDomingoetal.,

2000;MitscherlichandMarth,

1984;

ZibilskeandWeaver,1978)

Campylobacter

(Buswelletal.,

1998;Rollinsand

Colwell,

1986;Mitscherlichand

Marth1984;Blaseretal.,

1980)

Yersiniaenterocolitica

(KarapinarandGonul,1991;Chaoet

al.,

1988)

Escherichiacoli0157:H7

(Wangan

dDoyle,

1998;Tauxe1997;

Zhaoetal.,

1995;Cieslaketal.,

1993)

Water

1yr

>300d

~5

~6mo

1wk

4mo

>1yr

>300d

~30

~6mo

~4d

~10d

~84d

Soil

6mo

28wk

>1yr

>300d

~5

28wk

~2wk

>1yr

~100d

~30

~4wk

~1wk

~10d

~2d

Slurry

75d

13g/g l), ad fud heeera ffered pre f he DNA aga DNae a-vy. Bud DNA wa fud per lger ha free DNA he l evrme, ragg frm mh (Rere e al.,1993; Rmawk e al., 1993) a muh a 2 yr (Gehardad Smalla, 1999). Te meham a hugh pr-e l-ud DNA lude phyal pre frm awh eduleae, ad rp f eduleae lay, helaer reulg phyal epara ad ezyme frma-al hage ha dereae uleae avy (Demahe eal., 2001; Khaa ad Szky, 1992).

Bh hrmmal ad plamd DNA ud lay par-le repredly rafrmed aera erle l (Gal-lr e al., 1994). Te DNA ud hum ad wa al

erved rafrma f Bacillus subtilis (Creh adSzky, 1998), ad he add f mmrlle lay,kw d h DNA ad eduleae, reaed herafrma rae fB. subtilis(Lee ad Szky, 1999). Telkelhd f DNA perg l, parularly e hgher are lay ad hum ad, ad ree f aly frhe DNA rafrm ell, wuld ugge he ply frave l aera aqure ew gee maeral, ludggee ha fer a reae.

Detection of Antibiotic Resistance Genes in

the EnvironmentAurae ad meagful frma he peree ad

dema f a reae gee aera f fuda-meal mprae aeg peal healh rk ad evr-meal qualy. Te dee f pefi gee ad her aeralh are mpra mpe, ad reely develped eh-

que have ee appled fr dee f pefi reae geead aera aural evrme. I parular, he ue f m-leular ehque prvde rapd, eve, ad pefi deewhu he requreme fr aeral grwh ad la, whhfe pe a majr hallege gve he va ukw amuad fu f evrmeal mral pee (Nker e al.,2007). Cmmly ued mleular mral ehque are aed uque equee feaure f gee allw dee ad de-fia f mrrgam. Gee pre ad he ue f ply-merae ha rea (PCR) amplfia f ule ad wwdely ued eale dee ad quaa f lw level farge equee, ad ha eme a key predure he deead defia f aera ad gee frm a varey f evr-

me ludg l, waer, ad feal maeral (Malk e al., 2008;Kke e al., 2007; Amv e al., 2002; Chee-Safrd e al., 2001; Wag e al., 1996; Karh e al., 1995; Jeph e al., 1993).New apprahe lke mrarray ehlgy are eg develpedpefially dee ad defy amral reae l-al ad evrmeal aera (Frye e al., 2006; Call e al., 2003;Vlkhv e al., 2003). A ree udy ug a gee array apprahmulaeuly reeed fr he preee f 23 erayle re-ae gee ad 10 eryhrmy reae gee l ad fealample frm we fid he m prevale gee (Paere al., 2007). Mleular figerprg l ad r ehl-gy have falaed mre aurae ad eve mral hara-erza f mplex evrmeal ample ad ha prve e eeal prvdg mre frmave daa evrmealmrg ude (fr revew ee: Harwd ad Bukley, 2008; Wager e al., 2007). Te ree develpme f a umer fpre ha arge pefi a reae gee ha reaedhe umer f ude ha vegae he urree f heegee aural evrme. Suh ude lude dee fgee frm a-prdug aera, a well a gee rede he akgrud f aural ppula. Te fllwg ehghlgh he appla f mleular-aed mehd fr deead quaa f a reae gee aera adevrmeal ample.

Spefi lae f a a e haraer f he -

dury whh hey are ued, ad mulple a reaepheype prfile f aera have ee ued defy uref feal pllu (e.g., huma, pulry, ale, we) evr-meal ample (Olva ad Faulker, 2008; Parvee e al., 2006;Smp e al., 2002; Wgg e al., 1999; Plla e al., 1997;Kapar e al., 1990). May f hee ude fu aeralra f lal mprae ad d fully addre he har-aerza f ppula ha have aqured reae gee aural evrme. rumve ue relaed ulvaf aera, aaly f a reae gee a e ued

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haraerze he gee pl frm a evrme, wh pl-y f rakg he ure f feal ama urfae- adgrudwaer. Smlar he raegy ued mral dveryude, he arg p he deg f pre ad prmer frdee f a reae gee a ru phylgeeaaly. Spefi gee equee a e argeed fr dee, aduh a apprah ha ee ued demrae he dvery fa-rea gee pree we lag ad p effl ue.

Fr example, Amv e al. (2001, 2002) ad Chee-Safrd e al.(2001) fud he erayle reae effl ux gee (tetB, C, E,H, Y, Z) ad he rmal pre pre (RPP) gee (tetW,O, Q, M, S, , B(P), ad otrA) were all pree a gle wewae lag. Kke e al. (2007) deeed tet(M), (O), (Q), (W),(C), (H) ad (Z) ually ver a 3-yr perd grudwaeruderlyg w we farm. Furher, tet(W) equee deeed he grudwaer were early deal (99.8%) he fud he rrepdg lag. I he ame udy, he applaf he ame PCR prmer furher allwed he dee f uquead vel erayle reae gee equee. Ug mleular-aed dee, agrulural l were fud e a rh reervrf gee lely relaed he glypepde reae gee vanA

eer (Guardaa ad Ager, 2006).erayle reae gee have ee fud large um-

er lag effl ue. I a udy f a ale feedl lag,a real me PCR mehd wa ued dee ad quafy tet(O), (W), ad (Q) gee, ad rrelaed gee py umer erayle level (Smh e al., 2004). A ree udy hwedhe pere effe f maure ad he preee f ulfad-aze l aeral mmue, where he umer fulureale rea aera ad ulfamde reae geereaed (Heuer ad Smalla, 2007). A ree udy uggeedha maure rage ad reame have a large mpa per-ee ad dele f marlde-lamde-repgam Breae, where level ferm gee audae mpedwe maure were redued y everal rder f magudever level fud maure (Che e al., 2007).

Ree ude have repred la f a wde rage f a--rea aera revered frm l ad waer evrme(Dag e al., 2008; Oa ad LaPara, 2003; Ah e al., 2002;Eu e al., 2002; Chee-Safrd e al., 2001). A umer f lample ued hee ude were drely exped amal wae.Furhermre, equee f reae gee deeed aerallae were fud e deal equee fud lag ramal wae. Nklakpulu e al. (2005) reeed erayle-rea repmyee lae frm a rage f evrmealample fr xyerayle reae gee ad fud reae

gee erayle prdug lae. I al ewrhyha ulva raege, parularly fr ppula frm ev-rmeal ample, have hu far ly prvded a uderemaef aera, uggeg he ply ha a muh hgher dveryf a rea aera may ex u are ye auedfr. Furher ale, arhaea are w hugh e uquu may l evrme, ludg agrulural l (Gager eal., 2006; Leger e al., 2006). Arhaeal muldrug-reaeMarR famly pre were fud have mlar rarpalregula feaure he uerpar fud aera (Mya-

z e al., 2007). Furher, mua he arha Haloarculamarismortuiwere fud fer reae amy, a drug kw e ave aga aera, u vlve rmaldg e mlar fr drug uh a hlramphel ad l-damy (Blaha e al., 2008). Far le kw au l arhaeaad he exe f her reae meham r her ru- gee exhage wh he l meageme.

Evolution and Ecology of AntibioticResistance Genes

A a mpra ape f uderadg he mpa flad appla f amal wae l, he fial e fh revew aemp addre mplex ue f a re-ae a evluary ad elgal ex. Whle -efi evdee hw umeru dee f demaf lal le f pahge aera wh reae meha-m aqured y mua ad ele eve, he majryf a reae hugh e aqured hrugh herafer f gee frm her aera (Srum ad LAe-Lud,2002; Rer, 1998, 1998). I add aural reae

(e.g., lakg he drug arge r drug rapr yem), a- reae aera rede gee ha are eherhrmmal- r plamd-eded, wh he laer hugh empa meham m f drug urrely ue day(Bee, 2008). Te rage f a y a lae adhe rrepdg mde f reae exered y aera areummarzed ale 8. Te fllwg du deal hele f gee evdee ha uppr he rle f hrzalgee rafer he aural hry f a reae geeleadg he mre emprary era f a ue.

What is the Origin of Antibiotic Resistance Genes?

Amyee are aera mmly fud l, wh

memer mpred f may well-kw a-prdugpee. Crrepdgly, a-prdug ra al har-r reae meham pre aga he effe f he a- eg prdued. Over hree deade ag, wa repredha amglyde-avag ezyme amyee weremlar he pree lal lae f a-reaaera, uggeg a rg fr reae deerma (Be-vee ad Dave, 1973). May aeral-derved aprepara were al repred a gfia quaef DNA ad ha h DNA uld e rafrmed aera(Chakraary e al., 1990). We ad Dave (1993) firmedhe preee f a reae gee equee a umerf a prepara emplyed fr huma ad amal uead hyphezed ha he rapd develpme f mulple a- reae wa due he aqu f he DNA reduey aera. Hghly eve flureee dee ehquefirmed quae f DNA may a preparaf h reearh ad lal grade (Wegerauer e al., 2005).Mrever, m f hee prepara, he DNA wa pefi he a prdug ra ued he yhe pre,ad aed he rrepdg reae gee. Aemp demrae vv rafrma y hee a prepara-

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, hwever, were uueful (Wegerauer e al., 2005).Tee lleve repr uppred he ha a-prdug ra were he rgal ure f reae gee e laer fud a prdug aera.

Use of Phylogeny to Infer Evolutionary Origins of

Antibiotic Resistance Genes

Mleular phylgey he mparave aaly f gee e-quee, a he ulede r am ad level, ga frma- gee r pre evluary relahp. T aaly-

a e ued rae he evluary hry f areae gee, ad he rgam ha h he gee. Suh re-lahp have ee vegaed wh gee edg rm-al pre pre (RPP) ha fu a alerave preelga far ad fer reae erayle (C-ell e al., 2002, 2003). A ree phylgee aaly uggeedearly rahg eve ad depede le f dverfiaf a lea egh luer f RPP (Amv e al., 2001). Te d-vergee urred well efre he mder a era wh

da f rafer f a reae gee frm a- prdug ra pahge r mmeal aera. Aueque aaly wh a larger daaae f equee hwedhe mphyle rg (.e., deeded frm a gle mmaer) f he RPP gee, wh a early rahg eve epa-rag hem frm a eparae grup f elga far, EF-G,eded y hefusA gee (Amv ad Make, 2007). Severaldee f lely-relaed pee harrg dly dffer-e tetdeerma were al evde Several tetgee edgRPP, d frm he fud kw pee, have ee

fud he evrme u rrelaed kw ulvar(Yu e al., 2005), demrag he peal fr a wder ragef RPP gee dvery ha wha urrely kw.

A aher example f a phylgee apprah, a mlaraaly wa dued f he lally releva erm gee famly.Tee gee ede ezyme ha aalyze S-adeyl-L-meh-e-depede mehyla f a pefi adee redue he23S rRNA mleule, prvdg er pre f he rmefrm dg he marlde, lamde, ad repgram Blae f a, herey preveg he h f pr-

Table 8. Mechanisms o antibiotic action and resistance (rom Mathers et al., 2004; Skld, 2000; Prescott et al., 1999; Roberts, 1998; Cocito et al., 1997).

Antibiotic class (examples) Mechanism o antibiotic action Resistance mechanisms

Tetracyclines(Tetracycline, Chlortetracycline,Oxytetracycline)

Inhibition o protein synthesis (binds 30S ribosomalsubunit); intereres with aminoacyl-tRNA binding

Ribosomal protection protein E ux pumps Enzymatic (drug alteration)

Macrolides(Erythromycin, Tylosin,Carbomycin A)

MLSclass

Inhibition o protein synthesis (binds 50Sribosomal subunit, inhibits translocation opeptidyl tRNA

Methylation o 23S rRNA E ux pumps Enzymatic (drug inactivation)

Lincosamides

(Lincomycin, Clindamycin)

Inhibition o protein synthesis (binds 50S ribosomal

subunit, inhibits peptide elongation)

Methylation o rRNA

Mutation Enzymatic (drug inactivation)

Streptogramins(Virginiamycin)

Inhibition o protein synthesis (inhibits peptideelongation)

Target modication (rRNA or ribosomalprotein) E ux pumps Drug inactivation (lactonases)

Aminoglycosides(Gentamicin, Neomycin, Streptomycin)

Inhibition o protein synthesis (binds 30S ribosomalsubunit, inhibits translocation o petptidyl tRNA;misreading o mRNA)

Reduced uptake or decreased cellpermeability Altered ribosomal binding sites Production o aminoglycoside modiyingenzymes

Chloramphenicol Inhibition o protein synthesis (binds 50S ribosomalsubunit; inhibits peptidyl transerase)

Altered membrane permeability Enzymatic (aceyltranserase action toinactivate drug) Mutation (50S ribosomal subunit)

-Lactams (including Cephalosporins)

(Penicillin, Ampicillin, Carbenicillin,Cetiour)

Inhibition o cell wall (peptidoglycan) synthesis,

binds and inactivates PBPs

-lactamases (drug-modication enzymes)

Modied or low af nity PBPs E ux pumps

Sulonamides(Sulamethoxazole,Sulamethoxypyridine, Suladimethoxine)

Inhibition o olic acid synthesis (competitivelyinhibits DHPS by structural analogy withp-aminobenzoic acid)

New enzyme (mutation or mosaic dhps, highaf nity to PABA) Insertion o nucleotides (new DHPS)

Fluoroquinolones(Ciprooxacin, Dioxacin, Saraoxacin)

Inhibition o DNA replication and transcription(inhibits DNA gyrase and topoisomerase IV)

E ux pumps DNA gyrase-binding proteins Mutations (DNA gyrase,topoisomerase IV)

Polypeptides(Actinomycin, Bacitracin, Polymyxin B)

Disruption o cell membrane structure andpermeabilityOther (Axelsen, 2008)

Altered membrane structure

Ionophores(Monensin, Nystatin, Gramicidin A)

Disruption o transmembrane ion concentrationgradients

Enzymatic (drug degradation) Extracellular polysaccharides (excludes drugrom cell membrane)

Penicillin-binding proteins (PBPs) are enzymes involved in the terminal stages o assembling the cell wall during growth and division.

Dihydropteroate synthase catalyzes the condensation o p-aminobenzoic acid (PABA) and 7,8-dihydro-6-hyroxymethylpterin-pyrophosphate to ormdihydropteroic acid.

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e yhe. Aqu f hee mehylae gee feraeral reae eryhrmy. Te phylgey ferm geehw ha he rg f h gee famly plyphyle (.e.,havg mre ha e le f evlu) (Amv ad Make,2007) ad, a wh he RPP gee, here wa da fgee exhage ewee a-prdug ra ad he majry f her mmeal/pahge aera fud wh d-verge erm gee. Te mre ree phylgee aalye f he

RPP ad erm gee famle uppred lu preeed ude ha hwed evdee fr rafer f a re-ae gee frm a prdug aera huma- adamal-aaed aera (Lau e al., 2004).

Phylgee aalye f a reae gee al ug-ge a relavely ree me frame f rapd mveme f a- rea gee ewee axmally dverge mme-al ad pahge aera. erayle reae gee lketet(M) a e fud h Gram-pve ad Gram-egaveaera ad kw e raferred y rap Tn916,a mm mle gee eleme. Te tet(W) gee vruallydeal a rage f aeral pee (e.g., Megaspaera els-denii, Bifidobacterium longum, Roseburia hominis, Mitsuokella

multacida, ad Butyrivibrio fibrisolvens) uggeg very reelaeral gee exhage eve ewee aera frm huma,we, ad ale dgeve ra (Kazmerzak e al., 2006;Bara e al., 1999). Te pree gee meham rep-le fr he mveme ftet(W) ewee he gu eyemf dffere pee are preely ukw u preumaly -vlve a udefied mle eleme. Te va majry faera arryg tetgee are f eal r geal rg, adhrzal gee exhage ewee hee, a well a raeaera, derale.

Laeral gee rafer f he erm(B) ad erm(C) gee e-wee Gram-pve ad Gram-egave aera ha ee -daed (Amv ad Make, 2007). Aaly f he erm adtetgee Bacteroidesad her predma eal a-era uggeed ha hee gee have ee demaed rapdlyamg huma ppula hpal ad he mmuyver he pa hree deade (Shemaker e al., 2001), whhde wh he a era. Mleular aaly f hu-ma, we, ad pulryEnterococcus faecium lae ad hererm(B) gee al ugge ha hrzal exhage f a- reae gee mre mpra dema fa reae ha dre ram f rea ra(De Leeer e al., 2005).

Factors Contributing to Persistence and Dissemination

of Antibiotic Resistance GenesI ha ee geerally hugh ha he maeae f a

reae deerma mpe a addal meal aaeral ell ad ha reae gee wll e elmaed frm heppula e he eleve preure remved. Ireaed -dee f a rea aera are learly evde, hwever,mply remvg he ele preure de revere he ur-ree (Salyer ad Amle-Cueva, 1997). A umer f udehave hw adapa y aera amelrae he meal

maa drug reae (Ee e al., 2005; Ramadhaad Hegedu, 2005; Lek, 1997). Mrever, he aqu fa a reae geype may aually reae he fief era aera he aee f a eleve preure,ply allwg rapd emergee ad dema f a- reae a wrldwde ale (Lu e al., 2005; Ee e al.,2004). Te amelra f he fie requred maaa reae may e e f he rea why, fr example,

a reae gee per wld amal he aeef ele mped y he preee f a (Gllver e al.,1999). A reae a he e vewed a a elf-perpeu-ag pre, where he a-ueple geype emereplaed y rea geype he aee f ay a e-leve preure. Tu, he releae f a reae gee he evrme hugh e a ral rl p. Areawh hrally lw level f agrulural a ue had lwerfrequee f a reae gee (Oerlad e al., 1995).

Aher equee f prlged a uage uld eele f vel gee vara r rema ha may -fer hgher mmum hry era (MIC). Marema tet(O/W/O) vara were fir laed frmMegas-

phaera elsdeniifrm we (Sa ad Humphrey, 2003). Teprevuly haraerzed tet(32) gee frm a huma mme-al Clostridium p. wa al hw e a ma rema,tet(O/32/O) (Sa e al., 2005). Aaly f he pulhedtet(O) gee equee frm Campylobacter coliuggeed ha hgee reuled frm a dule-rver rema ad hulde dered a a tet(O/M/O) (Bahelr e al., 2004). Te re-ma vara f he gee appeared have hgher MIC frerayle, whh mgh expla he ele ad peree fhee ma rema (Sa e al., 2004). Tu, mme-al l aera may erve a h k ad ure fr exgad ew vara f a reae gee.

Whle he fual rle f a reae gee a-prdug aera vu (elf-pre agahe a yhezed), he preee ad fu f heegee aera frm her elgal he a evde.Numeru dee f a reae gee preum-aly a-free evrme ugge her drvg far plae maa hee fual gee wh ell. Oe plau-le explaa fr harrg hee gee may e arued her meal huekeepg fu efre he eed pefi-ally fr a reae meham. Ceraly, evr-me wh hry f drug expure, lw level f a auralgee pl f a reae gee may ex. Tee geemay per, ferrg a eleve advaage fr he h ell

aurally mpeve evrme uh a l, r -elereuled reae gee mlzg alg wh gee fr herele preure (Amv ad Make, 2007).

Mre ree ude have hed lgh he rle f mall re-dx-ave a, lke pheaze, whh are prdued he evrme y may pee fPseudomonas, ad erve aple umer f fu, ludg rle a eler hule aeral meral redu pahway fr eergy (Sam e al.,2006; Heradez e al., 2004; Heradez ad Newma, 2001).Te glypepde lemy wa al fud mulae dm-

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lary r-redu Shewanella oneidensisMR1 (Heradeze al., 2004). Te rle f effl ux pump meham vlved pre f ell frm a are hugh e requred mgae he x effe f veraumula f he hum adaalg eler hule, ahraque-2,6-dulfae (AQDS)(Shyu e al., 2002). AQDS, lke her eler-hulg m-pud, ha ruural mlare arma a lkeerayle, dxru, ad he pheaze pyya (Her-

adez ad Newma, 2001). Tee le f udy ugge a-ural a prdued l y may aera have lkelyevlved wh aeral ell meal fu, ad uggereae gee have al evlved ardgly. Te furher ef-fe aural mral fu frm he added preee fa ad reae gee due agrulural pu are kw ad a ly e hyphezed.

Co-selection of Antibiotic Resistance Genes

May a reae gee rede large elf-ra-mle gee eleme apale f arryg mulple gee,ludg he edg a-, heavy meal-, ad de-reae. Te phyal lk ewee he jugave la f R

plamd ad reae heavy meal wa repred alm 40yr ag (Smh, 1967). Ampll- ad merury-rea Bacil-lusra were fud early x me mre freque ed-me wh a lg hry f heavy meal expure (meye al., 1978). Te gee lkage ewee a reaead merury reae eeraera wa hw vlvehe gee eleme Tn21, whh ede a merury-reaeper, rap fu, ad reae repmy-/pemy ad ulphamde (Leer e al., 1999).Te reae gee are arred aera a egr, whh a prale, raferale, mul-gee aee. Suh mehamf -ele ugge he peal fr a gle rafer eve reul mulple reae aqu y a aerum. I hafurher ee hw ha ellular re a due he mlyf rap ad er equee (Ilve e al., 2001; Levye al., 1993). Te DNA-damagg age uh a he ala f flurqule due a majr aeral re repemeham, ur aug a reae he rae f hrzalrafer f a reae gee y mre ha 300-fld (Be-aer e al., 2004). Sre repe-dug a may al-ele fr her a reae gee ha are phyallylked mle gee eleme (Hag e al., 2004).

SummaryTe mpa reulg frm agrulural ue f a

ad he prae f lad appla f amal wae ev-rmeal qualy ad healh rk peal mpleelylear, ale here are demraed lk reaed ad a-eleraed dee f a rea aera. Te phe-me, hwever, a mple relahp f aue adeffe. Wha evde he myrad mplexy f a adlgal meham, ad he elgal era ha aur a umeru p alg he ure f a uead dpal f lvek wae l evrme, egg

wh ery f a amal gu yem. Regularyape relaed ued ue f lad appla fr waemaageme amal prdu ha real urre erfr ure (N, P) lad l; he praal mpa f ladga redue ad reae gee ye kw. Telleve exama f pefi meham ha affe hefae f mpud, mrrgam, ad he gee pl (Fg.1), wll prvde a eer uderadg f he rue mpa f

lad appla f effl ue, a well a he geeral aure f hemral ad mleular elgy f a reae.

Feld frma he fae ad rapr f a lllmed, u geeral, lw amu have ee deeed l adwaer evrme, ludg he preee f reakdw mea-le. Predve meaure fr lue ad aera rapr lad waer have reled exg mdel, whh d adequaelypred ama, ad dae a lear eed fr a larger daa-ae develp ad eer frm mdel. Te phyhem-al haraer f he l evrme are lkely flueempud peree, aeral urvval, ad gee mehama wrk. rae amu f a r her mpud (e.g.,heavy meal) uld a a ele preure fr maeae ad

(-) rafer f a reae gee.Whle he half-lve f a maure are relavely

hr, rema ple ha drug redue may exer effe lgal fu wh aeral ppula pree l. Sude have hw appla f amal maure la readly lead grudwaer ama wh feal a-era. Te aqu f a reae, hwever, appear pa a dvere phylgee rage f aera, ludg heave l ad waer evrme. Phylgee aalyef gee vlved erayle ad eryhrmy reaedemrae he evlu f hee gee ver me, ad ug-ge ha ag reae gee frm a-prdugaera a majr meham f reae aqu ev-de a rad rage f aera. Reae gee have eemaaed aera efre he mder a era, evehugh he rg ad purpe f hee gee ye lear.Te exa meham rug a reaegee aqu ad maeae aural evrmeare ye well ealhed, hwever, a reag umer fude uppr laeral gee rafer eve. Aqu f a- reae hrugh meham f eleve muaad laeral gee rafer may e ag er wh heraural meham f gee adapa amg a dvererage f aera aural l ad waer evrme.

ReferencesAHI. 2001. Survey hw dele a ue amal. Avalale a

hp://www.ah.rg/e.ap?ed=694 (verfied 16 Fe. 2009).Amal Healh I., Wahg, DC.

Alexy, R., . Kmpel, ad K. Kmmerer. 2004. Aeme f degrada f18 a he Cled Ble e. Chemphere 57:505512.

Allare, S.E., J. Del Call, ad V. Jueau. 2006. Srp ke fhlrerayle ad yl ady lam ad heavy lay l. J.Evr. Qual. 35:969972.

Amle-Cueva, C.F., ad M.E. Churel. 1992. Baeral plamd ad geeflux. Cell 70:189199.

Amv, R.I., J.C. Chee-Safrd, N. Garrgue, B. eferedege, I.J. Krapa,

8/3/2019 Ind 44197785

18/23


B.A. Whe, ad R.I. Make. 2002. Develpme, valda, adappla f prmer fr dee f erayle reae geeedg erayle effl ux pump gram-egave aera. Appl.Evr. Mrl. 68:17861793.

Amv, R.I., N. Garrgue-Jeajea, ad R.I. Make. 2001. Mleularelgy f erayle reae: Develpme ad valda fprmer fr dee f erayle reae gee edg rmalpre pre. Appl. Evr. Mrl. 67:2232.

Amv, R.I., ad R.I. Make. 2007. Evlu ad elgy f areae gee. FEMS Mrl. Le. 271:147161.

Adrem, A. 2003. Cmmeal flra may play key rle preadga reae. ASM New 69:601607.

Adrew, R.E., Jr., W.S. Jh, A.R. Guard, ad J.D. Marv. 2004.Survval f eer ad 916-lke jugave rap l.Ca. J. Mrl. 50:957966.

Ah, R.J., B. Mauk, ad M. Mrga. 2002. A reae f Gram-egave aera rver, Ued Sae. Emerg. Ife. D. 8:713716.

Ahelfrd, K.E., M.J. Day, ad J.C. Fry. 2003. Elevaed audae faerphage feg aera l. Appl. Evr. Mrl.69:285289.

Axele, P.H. 2008. A ha pre mdel f plypepde a a.Bphy. J. 94:15491550.

Azadpur-Keeley, A., B.R. Faulker, ad J.-S. Che. 2003. Mveme adlgevy f vrue he uurfae. OH EPA/540/S-03/500. U.S. Evr.Pre Agey, Nal. Rk Maage. Re. La., Ca, OH.

Bahl, M.I., S.J. Sree, L.H. Hae, ad .R. Lh. 2004. Effe ferayle rafer ad ealhme f he erayle-dule

jugave rap Tn916 he gu f g ra. Appl.Evr. Mrl. 70:758764.

Balmer, M.E., K.-U. G, ad R.P. Shwarzeah. 2000. Phlyrafrma f rga pllua l urfaeA expermealapprah. Evr. S. ehl. 34:12401245.

Bara, .M., K.P. S, ad H.J. Fl. 1999. Evdee fr ree ergeerrafer f a ew erayle reae gee, tet(W), laed frmButyrivibrio fibrisolvens, ad he urree ftet(O) rumal aera.Evr. Mrl. 1:5364.

Barr, V., K. Barr, M.R. Mllar, ad R.W. Laey. 1986. -Laam areae he frequey f plamd rafer Staphylococcus aureus. J.

Amr. Chemher. 17:409413.

Bahelr, R.A., B.M. Pear, L.M. Fr, P. Guerry, ad J.M. Well. 2004.Nulede equee ad mpar f w large jugave plamdfrm dffere Campylobacterpee. Mrlgy 150:35073517.

Bauer, B., K. Haelma, W. Shlmme, ad B. Je. 1996. Gee

rafrma frehwaer: Escherichia coli ale develp auralmpeee. Appl. Evr. Mrl. 62:36733678.

Beaer, J.W., B. Hhhu, ad M.K. Waldr. 2004. SOS repe prmehrzal dema f a reae gee. Naure (Ld)427:7274.

Beaue, J. 2004. Seleed drug ld mare: A revew f evrmealdeerma, urree ad prpere f prpal uae. red

Aal. Chem. 23:753761.

Beegle, D. 1997. Ug mped dary maure. Adv. Dary ehl.9:6772.

Bee, P.M. 2008. Plamd eded a reae: Aqu adrafer f a reae gee aera. Br. J. Pharmal.153:53475357.

Bevee, R., ad J. Dave. 1973. Amglyde a-avagezyme amyee mlar he pree lal lae fa-rea aera. Pr. Nal. Aad. S. USA 70:22762280.

B, G., ad R.W. Harvey. 1992. rapr f pahge hrugh l adaqufer. p. 103124. In R. Mhell (ed.) Evrmeal mrlgy.

Wley-L, New Yrk.

Blaha, G., G. Grel, S.J. Shreder, P.B. Mre, ad .A. Sez. 2008.Mua ude he amy-dg e a make rmedrug-rea. J. Ml. Bl. 379:505519.

Blaer, M.J., H.L. Hardey, B. Pwer, ad W.L. Wag. 1980. Survval fCampylobacter fetusup.jejuni lgal mleu. J. Cl. Mrl.11:309313.

Blum, S.A.E., M.G. Lrez, ad W. Wakeragel. 1997. Meham f reardedDNA degrada ad prkary rg f DNae erle l.Sy. Appl. Mrl. 20:513521.

Be, J., L. Ala, J. Bagger, V. Mgelme, D.L. Bagge, ad J.E.

Ole. 2005. Survval f Escherichia coli ad Salmonella typhimurium lurry appled lay l a Dah we farm. Prev. Ve. Med.69:213228.

Bl, D.J., C.M. Byre, J.J. Sherda, D.A. MDwell, ad I.S. Blar. 1999.Te urvval haraer f a -xge ra f Escherichia coliO157:H7. J. Appl. Mrl. 86:407411.

Bh, M.G., W.H. Jeffrey, ad R.V. Mller. 2001. ReA expre repe lar UVR he mare aerum Vibrio natriegens. Mr. El.42:531539.

Bxall, A.B.A., P. Blakwell, R. Cavall, P. Kay, ad J. ll. 2002. Te rpad rapr f a ulphamde a l yem. xl. Le.131:1928.

Bxall, A.B.A., L.A. Fgg, P.A. Blakwell, P. Kay, E.J. Pemer, ad A.Crxfrd. 2004. Veerary mede he evrme. Rev. Evr.Cam. xl. 180:191.

Bxall, A.B.A., P. Jh, E.J. Smh, C.J. Slar, E. Su, ad L.S. Levy.2006. Upake f veerary mede frm l pla. J. Agr.Fd Chem. 54:22882297.

Braa, A.D., E. He, ad .R. Callaway. 2005. Evlu f fdredpahge va emperae aerphage-medaed gee rafer.Fdre Pahg. D. 2:287303.

Brw, H., C. Cahaya, ad W.D. Hard. 2004. Phage ad he evluf aeral pahge: Frm gem rearrageme lygever. Mrl. Ml. Bl. Rev. 68:560602.

Buherger, W.W. 2007. Nvel aalyal predure fr reeg f drugredue waer, wae waer, edme ad ludge. Aal. Chm. Aa593:129139.

Burkhard, M., C. Samm, C. Waul, H. Sger, ad S. Muller. 2005. Surfaeruff ad rapr f ulfamde a ad raer mauredgralad. J. Evr. Qual. 34:13631371.

Buwell, C.M., Y.M. Herlhy, L.M. Lawree, J.. MGugga, P.D. Marh,C.W. Keevl, ad S.A. Leah. 1998. Exeded urvval ad pereefCampylobacter pp. waer ad aqua film ad her deey mmufluree-ady ad rRNA ag. Appl. Evr.Mrl. 64:733741.

Ca, P., Q. Huag, X. Zhag, ad H. Che. 2006a. Adrp f DNA lay meral ad varu lldal parle frm a Alfil. Sl Bl.Bhem. 38:471476.

Ca, P., Q.-Y. Huag, ad X.-W. Zhag. 2006. Iera f DNA wh laymeral ad l lldal parle ad pre aga degraday DNae. Evr. S. ehl. 40:29712976.

Call, D.R., M.K. Bakk, M.J. Krug, ad M.C. Rer. 2003. Idefygamral reae gee wh DNA mrarray. Amr.

Age Chemher. 47:32903295.Campagl, E.R., K.R. Hh, A. Karpa, C.S. Ru, D.W. Klp,M.. Meyer, J.E. Eea, R.W. Currer, K. Smh, K.M. Tu, ad M.MGeeh. 2002. Amral redue amal waer ad waerreure prxmal large-ale we ad pulry feedg pera.S. al Evr. 299:8995.

Crme, H., F. Bure, P. Sme, ad .M. Vgel. 2004. Ilaf lghg-mpee l aera. Appl. Evr. Mrl.70:63426346.

Chakraary, A.N., S.G. Dadar, M. Gagul, ad D. Chapadhyay. 1990.DNA a ama a ad apay rafrmaera drug reae. Ida J. Exp. Bl. 28:5862.

Chadler, D., I. Farra, ad J. Crave. 1981. Peree ad dru fpllu dar aera lad ued fr dpal f pggery effl ue.

Appl. Evr. Mrl. 42:453460.

Cha, W.L., R.J. Dg, ad R.S. Che. 1988. Survval fYersinia entercolitica he evrme. Ca. J. Mrl. 34:753756.

Chee-Safrd, J.C., R.I. Amv, I.J. Krapa, N. Garrgue-Jeajea, ad R.I.Make. 2001. Ourree ad dvery f erayle reae gee lag ad grudwaer uderlyg w we prdu fale.

Appl. Evr. Mrl. 67:14941502.

Che, I., ad D. Duau. 2004. DNA upake durg aeral rafrma.Na. Rev. 2:241249.

Che, J., Z. Yu, F.C. Mhel, Jr., . Wum, ad M. Mrr. 2007.Develpme ad appla f real-me PCR aay fr quafiaf erm gee ferrg reae marlde-lamde-repgram B lvek maure ad maure maageme yem.

Appl. Evr. Mrl. 73:44074416.

Cherry, J.A., B.L. Parker, K.R. Bradury, .. Ea, M.B. Gkwz, D.J.

8/3/2019 Ind 44197785

19/23


Har, ad M.A. Brhard. 2007. Cama rapr hrughaquard: A ae-f-he-ee revew. Amera Waer Wrk A.,Dever, CO.

Celak, P.R., .J. Barre, P.M. Grffi , K.F. Gehemer, G. Beke, J.Buffi g, ad M.G. Smh. 1993. Escherichia coli0157:H7 fefrm a maured garde. Lae 342:367.

Clke, M.R.J., A.D. Mllard, W.H. Wl, ad N.H. Ma. 2003.Eapda f h DNA y aerphage feg mareSynechococcusra. FEMS Mrl. El. 46:349352.

C, C., M. D Gamaa, E. Nye, ad P. Vauffel. 1997. Ihf pre yhe y repgram ad relaed a. J.

Amr. Chem. 39(Suppl. A):713.

Cell, S.R., C.A. reer, G.P. D, E. Efeld, D.E. aylr, ad K.H.Nerhau. 2003. Meham f e(O)-medaed erayle reae.EMBO J. 22:945953.

Cell, S.R., C.A. reer, U. Selzl, E. Efeld, D.E. aylr, ad K.H. Nerhau.2002. Te erayle reae pre e(O) perur he frmaf he rmal dedg ere. Ml. Mrl. 45:14631472.

C, C., D.I. Ma, ad S. Quey. 2006. Redu f dar adpahge mrrgam y pyhrphl aaer dge we lurre. Breur. ehl. 97:686691.

Ca, M.A., .R. Whehead, ad R.L. Zelwager. 2003. Ila,haraerza ad mpar f aera frm we faee admaure rage p. Evr. Mrl. 5:737745.

Creh, C., ad G. Szky. 1998. Bdg f DNA hum ad: Effe rafrma fBacillus subtilisad reae DNae. Sl Bl.Bhem. 30:10611067.

Crmwell, G.L. 2001. Amral ad prmral age. p. 401426.In A. Lew ad L. Suher (ed.) Swe ur. 2d ed. CRC Pre,Ba Ra, FL.

Daae, L., J. Mla, E. Berry, ad M. Sadwky. 1996. Ifluee f earhwrmavy gee rafer frm Pseudomonas fluorescens dgeu laera. Appl. Evr. Mrl. 62:515521.

Dag, H., J. Re, L. Sg, S. Su, ad L. A. 2008. Dvere eraylerea aera ad reae gee frm aal waer f JazhuBay. Mr. El. 55:237246.

Daugh, C.G. 2004. PPCP he evrme: Fuure reearhegg wh he ed alway md. p. 463495. In K. Kmmerer (ed.)Pharmaeual he evrme. 2d ed. Sprger, New Yrk.

DCa, V.M., K.M. MGra, D.W. Hughe, ad G.D. Wrgh. 2006. Samplghe a reme. See (Wahg, DC) 311:374377.

De Leeer, E., A. Marel, E.M. DeGraef, J. p, P. Buaye, F. Haeeruk, R.Wllem, ad A. Deere. 2005. Mleular aaly f huma, pre,

ad pulryEnterococcus faecium lae ad her erm(B) gee. Appl.Evr. Mrl. 71:27662770.

Demahe, S., F. Berlla, F. Bure, R. Nal, A. Sallad, P. Aurl, .M. Vgel,ad P. Sme. 2001a. Larary-ale evdee fr lghg-medaedgee rafer l. Appl. Evr. Mrl. 67:34403444.

Demahe, S., L. Jeur-Mrzer, H. Ququampx, ad P. Sme. 2001.Evalua f lgal ad phyal pre aga uleae degradaf lay-ud plamd DNA. Appl. Evr. Mrl. 67:293299.

Demahe, S., E. Kay, F. Gurre, ad P. Sme. 2001. Nauralrafrma fPseudomonas fluorescensadAgrobacterium tumefaciens l. Appl. Evr. Mrl. 67:26172621.

DGva, G., J. Nel, I. Pepper, ad N. Slar. 1996. Gee rafer fAlcaligenes eutrophus JMP134 plamd pJP4 dgeu l repe.Appl. Evr. Mrl. 62:25212526.

D, A.M., ad M.K. Skpf. 2000. Te ke f xyerayledegrada dezed waer uder varyg emperaure, pH, lgh,urae, ad rga maer. J. Aqua. Am. Healh 12:246253.

Dllver, H.A.S., ad S.C. Gupa. 2008. A le frm upreedmaure kple. J. Evr. Qual. 37:12381244.

Dllver, H., K. Kumar, ad S. Gupa. 2007. Sulfamehaze upake y plafrm maure-ameded l. J. Evr. Qual. 36:12241230.

Dhe, A.L. 1984. Bhemal ude he fae f me amalad he evrme. J. Am. S. 58:15281539.

Due-Ppulare, F., P. reu-Cu, I. Daa, A. Adrem, ad P.Curval. 1991. Idule rafer f jugave rap Tn1545frm Enterococcus faecalis Listeria monocytogenes he dgeve raf g me. Amr. Age Chemher. 35:185187.

Elmud, G.K., S.M. Mrr, D.W. Gra, ad M.P. Nev. 1971. Rlef exreed hlrerayle mdfyg he demp pre

feedl wae. Bull. Evr. Cam. xl. 6:129135.Ee, V.I., P.M. Bee, D.M. Lvermre, ad L.M. Hall. 2004. Ehaeme

f h fie y he ul2-dg plamd p9123 he aee feleve preure. J. Amr. Chemher. 53:958963.

Ee, V.I., A.A. Dell, G.R. Dav, S.L. Hayward, J.M. Re, ad P.M.Bee. 2005. Aeme f he fie mpa Escherichia colifaqu f a reae gee eded y dffere ype fgee eleme. J. Amr. Chemher. 56:544551.

Eu, N., L. Armea, ad J. Ike. 2002. A reae l adwaer evrme. I. J. Evr. Healh Re. 12:133144.

Fema, S.E., ad J.C. Mahe, III. 1978. Draf evrmeal mpaaeme: Suherapeu aaeral age amal feed. Bureau fVeerary Mede. Fd ad Drug Adm., Rkvlle, MD.

Frye, J.G., . Jee, F. Lg, G. Rdeau, S. Prwllk, M. MClellad, C.R. Jak, M. Egle, ad P.J. Fedrka-Cray. 2006. DNA mrarraydee f amral reae gee dvere aera. I. J.

Amr. Age 27:138151.Fulhage, C.D., ad D. P. 2005. Swe maure maageme yem

Mur. Avalale a hp://www.muexe.mur.edu/xplr/evqual/eq0350.hm (verfied 16 Fe. 2009).

Gallr, E., M. Bazzalup, L. Dal Ca, R. Fa, P. Naper, C. Ver,ad G. Szky. 1994. rafrma fBacillus subtilisy DNA ud lay -erle l. FEMS Mrl. El. 15:119126.

Garer, S., E. Urh, R. Alexy, ad K. Kmmerer. 2007a. Aaer had degrada f a ISO e heme. Chemphere66:18391848.

Garer, S., E. Urh, R. Alexy, ad K. Kmmerer. 2007. Ulmae

degrada ad elma f a here e.Chemphere 67:604613.

Gager, A., D. Elhva, M. Larez, D. Wager, J.C. Muh, ad M.Shler. 2006. Sruure ad fu f arhaeal mmue aural ad agrulurally ued l eyem. Gephy. Re. Ar. Vl.8, 06426. Eurpea Geee U, Sraurg Cedex, Frae.

Gavalh, J., ad S.E. Kaz. 1994. Te peree f feal-re a l. J. AOAC 77:481485.

Gehard, F., ad K. Smalla. 1999. Mrg field releae f geeallymdfied ugar ee fr peree f rage pla DNA adhrzal gee rafer. FEMS Mrl. El. 28:261272.

Gera, C.P., ad G. B. 1984. Mral pllua; her urvval adrapr paer grudwaer. p. 6588. In G. B ad C.P. Gera(ed.) Grudwaer pllu mrlgy. Jh Wley & S, New Yrk.

Gera, C.P., ad J.B. Re. 1990. Vrue ure ad drkg waer. p.380396. In G.A. MFeer (ed.) Drkg waer mrlgy. Prgre

ad ree develpme. Sprger-Verlag, New Yrk.Ghh, D., K. Ry, K.E. Wllam, D.C. Whe, K.E. Wmmak, K.L.Sulee, ad M. Radevh. 2008. Prevalee f lygey amg laera ad preee f 16S rRNA ad rzN gee vral-mmuyDNA. Appl. Evr. Mrl. 74:495502.

Glhr, M.J., C. Grek, D.B. Wallga, G.W. Bera, D.G. Rley, adP.S. Tre. 2007. Te peal rle f eraed amal feedgpera feu deae epdem ad a reae.Evr. Healh Perpe. 115:313316.

Gllver, M.A., M. Bee, M. Beg, S.M. Hazel, ad C.A. Har. 1999. Areae fud wld rde. Naure (Ld) 401:233234.

Gz, A., ad K. Smalla. 1997. Maure ehae plamd mlza adurvval fPseudomonas putida rdued field l. Appl. Evr.Mrl. 63:19801986.

Gyal, S.M. 1983. Idar f vrue. p. 211230. In G. Berg (ed.) Vralpllu f he evrme. CRC Pre, Ba Ra, FL.

Gua, .Y., ad R.A. Hlley. 2003. Pahge urvval we maureevrme ad ram f huma eer lleA revew. J.Evr. Qual. 32:383392.

Guardaa, L., ad Y. Ager. 2006. Gee hmlgu glypepdereae vanA are wdepread l mral mmue. FEMSMrl. Le. 259:221225.

Gu, X., J. Che, R.E. Brake, ad L.R. Beuha. 2002. Survval fSalmonella mae red a hgh relave humdy, l, ad mae a wh l. J. Fd Pr. 65:274279.

Guaf, R.H., ad R.E. Bwe. 1997. A ue amal agrulure.J. Appl. Mrl. 83:531541.

Haak, B.J., ad R.E. Adrew. 2000. Ila f 916-lke jugaleleme frm we l effl ue. Ca. J. Mrl. 46:542549.

8/3/2019 Ind 44197785

20/23


Hallg-Sree, B., S.N. Nele, P.F. Lazky, R. Igerlev, H.C. Hle Lzhf,ad S.E. Jrgee. 1998. Ourree, fae ad effe f pharmaeualuae he evrmeA revew. Chemphere 36:357393.

Hamher, G., H.. Pawelzk, H. Hper, ad H. Nau. 2005. Dffereehavr f erayle ad ulfamde ady l afer repeaedferlza wh lqud maure. Evr. xl. Chem. 24:861868.

Hamher, G., S. Szey, H. Hper, ad H. Nau. 2002. Deerma fpere erayle redue l ferlzed wh lqud maure yhgh-perfrmae lqud hrmagraphy wh elerpray zaadem ma permery. Aal. Chem. 74:15091518.

Hazawa, Y., O.C. Ihgur, ad G. Sa. 1984. A-rea lfrm he wae f pggere ad dary farm. Japa. J. Ve. S. 46:363372.

Harper, L.A., R.R. Sharpe, .B. Park, A. De Vher, O. va Cleempu, adF.M. Byer. 2004. Nrge ylg hrugh we prdu yem:

Amma, drge, ad ru xde em. J. Evr. Qual.33:11891201.

Harwd, C., ad M. Bukley. 2008. Te uhared mral wrld:Mre ad her ave he evrme. Amera Aademy fMrlgy, Wahg, DC.

Hag, P.J., S.M. Reerg, ad A. Slak. 2004. A-dued laeralrafer f a reae. red Mrl. 12:401404.

Hauer, M., ad S. Wuerz. 1999. Hgh rae f juga aeralfilm a deermed y quaave u aaly. Appl. Evr.Mrl. 65:37103713.

Heradez, M.E., A. Kappler, ad D.K. Newma. 2004. Pheaze adher redx-ave a prme mral meral redu.

Appl. Evr. Mrl. 70:921928.

Heradez, M.E., ad D.K. Newma. 2001. Exraellular eler rafer.Cell. Ml. Lfe S. 58:15621571.

Heuer, H., E. Krgerreklefr, E.M.H. Wellg, S. Ega, J.D. va Ela, L. vaOvereek, J.M. Cllard, G. Gullaume, A.D. Karagu, .L. Nklakpulu,ad K. Smalla. 2002. Geam reae gee evrmeal aera:Prevalee ad rafer. FEMS Mrl. El. 42:289302.

Heuer, H., ad K. Smalla. 2007. Maure ad ulfadaze yergallyreaed aeral a reae l ver a lea w mh.Evr. Mrl. 9:657666.

Hy, K., L.D. MKay, P. Jrgee, M. Lezewk, ad C.P. Gera. 1996. Fraureaperure meaureme ad mgra f lue, vrue, ad mmleree a lum f lay-rh ll. Grud Waer 34:10651075.

Hrh, R., . ere, K. Haerer, ad K.L. Kraz. 1999. Ourree f a he aqua evrme. S. al Evr. 225:109118.

Herer, J.D., A.A. Arld, D.A. Kuzyka, A. Shuya, C.S. Ward, M.G.Sauer, A. Gzahew, .M. Hhk, .J. Flemg, ad S. Jh.

2005. Effe f ulehal UVA rrada avy level f xdavedefee ezyme ad pre xda Escherichia coli. J. Phhem.Phl. B Bl. 81:171180.

Hu, J.P., ad J.W. Ple. 1969. Ke ad meham f degrada fampll lu. J. Pharm. S. 58:447454.

Hwell, J.M., M.S. ye, ad P.L. Crelu. 1995. Feal aera agrulural waer f he luegra reg f Keuky. J. Evr. Qual.24:411419.

Huag, C.-H., J.E. Reew, K.L. Smey, K. Pk, ad D.L. Sedak.2001. Aeme f peal a ama waer adprelmary urree aaly.p. 4657. In Pr. f he 2d I.Cf. Pharmaeual ad Edre Drupg Chemal

Waer, Meapl, MN. Oer 2001. Nal. Grudwaer A.,Weervlle, OH.

Huh, M.L., L.D. Waler, A. Mre, K.M. Crke, ad S.M. Avery.2004. Effe f legh f me efre rpra urvval fpahge aera pree lvek wae appled agrulural

l. Appl. Evr. Mrl. 70:51115118.Ilve, H., R. Hrak, ad M. Kvaar. 2001. Ivlveme f gma(S)

arva-dued rap f Pseudomonas putida rap4652. J. Baerl. 183:54455448.

Igerlev, F., ad B. Hallg-Sree. 2001. Bdegradaly f merdazle,laqudx, ad yl ad frma f yl degrada prdu aer l-maure lurre. Exl. Evr. Safey 48:311320.

Iue f Mede. 1989. Huma healh rk wh he uherapeuue f pell r erayle amal feed. Nal. Aademy Pre,

Wahg, DC.

Iaa, R.E., ad M.E. rree. 2002. Te rle f a agrulure.Amera Aademy f Mrlgy, Wahg, DC.

Jae, P., ad L. Bergld. 1988. Peree f xyerayle edmefrm fih farm. Aquaulure 70:365370.

Jag, X., J. Mrga, ad M.P. Dyle. 2002. Fae fEscherichia coliO157:H7 maure-ameded l. Appl. Evr. Mrl. 68:26052609.

Jag, S.C., ad J.H. Paul. 1998. Gee rafer y radu he mareevrme. Appl. Evr. Mrl. 64:27802787.

Jeph, K.L., C.P. Gera, ad I.L. Pepper. 1993. Plymerae ha rea fvale aeral pahge. Appl. Evr. Mrl. 59:35133515.

Karapar, M., ad S.A. Gul. 1991. Survval f Yersinia enterocolitica adEscherichia coli prg waer. I. J. Fd Mrl. 13:315319.

Karh, H.A., A. Shwarzkpf, ad H. Shmd. 1995. Amplfia mehd dag aerlgy (eleed example). J. Mrl. Mehd23:5573.

Kapar, C.W., J.L. Burge, I.. Kgh, ad R.R. Clwell. 1990. Areae dexg f Escherichia coli defy ure f fealama waer. Ca. J. Mrl. 36:891894.

Kay, P., P.A. Blakwell, ad B.A. Bxall. 2004. Fae f veerary a a marpru le draed lay l. Evr. xl. Chem.23:11361144.

Kay, P., P.A. Blakwell, ad B.A. Bxall. 2005. rapr f veerarya verlad flw fllwg he appla f lurry aralelad. Chemphere 59:951959.

Kazmerzak, K.A., H.J. Fl, ad K.P. S. 2006. Cmparave aalyf equee flakg tet(W) reae gee mulple pee f guaera. Amr. Age Chemher. 50:26322639.

Kewk, B.H., ad C.P. Gera. 1980. Vrue grudwaer. Evr. S.ehl. 14:12901297.

Khahaura, G.G. 1998. Agrulural ue f a ad he evlu adrafer f a-rea aera. Ca. Med. A. J. 159:11291136.

Khaa, M., ad G. Szky. 1992. rafrma fBacillus subtilisy DNAud mmrlle ad effe f DNae he rafrmgaly f ud DNA. Appl. Evr. Mrl. 58:19301939.

Key, H.J., C. Hagedr, ad E.L. MCy. 1978. Ue f feal rep adar f pllu l. Appl. Evr. Mrl. 35:711717.

Km, Y.H., K. Pak, J.V. Phulur, ad C.E. Cergla. 2004. Meralzaf eryhrmy A aquaulure edme. FEMS Mrl. Le.234:169175.

Kke, S., I.G. Krapa, H.D. Olver, A.C. Yaarell, J.C. Chee-Safrd,R.I. Amv, ad R.I. Make. 2007. Mrg ad ure rakgf erayle reae gee lag ad grudwaer adjae we prdu fale ver a 3-year perd. Appl. Evr.Mrl. 73:48134823.

Klp, D.W., E.. Furlg, M.. Meyer, E.M. Turma, S.D. Zaugg, L.B.

Barer, ad H.. Bux. 2002. Phamaeual, hrme, ad herrga waewaer ama US Sream, 19992000: A NaalReaae. Evr. S. ehl. 36:12021211.

Klz, A.C., .B. Mrma, S.K. Og, K.D. Sgg, ad E.A. Dugla.2005a. Degrada ad meale prdu f yl aaerad aer we-maure lag. Waer Evr. Re. 77:4956.

Klz, A.C., S.K. Og, ad .B. Mrma. 2005. Srp f yl we maure. Chemphere 60:284289.

Krapa, I.G., S. Kke, M.. Meyer, D.D. Sw, S.-F.J. Chu, R.I. Make, W.R. Ry, ad J.C. Chee-Safrd. 2004. Lg-erm mrg fhe urree f a redue ad a reae gee grudwaer ear we fieme fale. p. 158174. In Pr.f he 4h I. Cf. Pharmaeual ad Edre DrupgChemal Waer, Meapl, MN. Oer 2004. NaalGrudwaer A., Weervlle, OH.

Kumar, K., S.C. Gupa, S.K. Bad, Y. Chader, ad C.J. Re. 2005.A upake y pla frm l ferlzed wh amal maure. J.Evr. Qual. 34:20822085.

Kmmerer, K. 2004. Reae he evrme. J. Amr. Chem.54:311320.

Kmmerer, K., A. Al-Ahmad, ad V. Merh-Suderma. 2000. Bdegradalyf me a, elma f he gexy ad affe f wae

waer aera a mple e. Chemphere 40:701710.

Larey, F.J., K.E. Bukley, X. Ha, ad W.P. MCaughey. 2006. Freh,kpled, ad mped eef ale feedl maure: Nure levelad ma alae emae Alera ad Maa. J. Evr. Qual.35:18441854.

Lau, S.K., P.C. W, A.P. , A.. Lau, ad K.Y. Yue. 2004. Lak f evdeeha DNA a prepara a ure f a reae

8/3/2019 Ind 44197785

21/23


gee aera frm amal r huma ure. Amr. AgeChemher. 48:31413146.

Lee, G.-H., ad G. Szky. 1999. rafrma ad urvval f dr,repe, ad rafrma fBacillus subtilis in vitro ad l. SlBl. Bhem. 31:14991508.

Lehma, J., Z. La, C. Hylad, S. Sa, D. Slm, ad Q.M. Keerg.2005. Lg-erm dyam f phphru frm ad ree maure-ameded l. Evr. S. ehl. 39:66726680.

Leger, S., . Urh, M. Shler, L. Shwrk, J. Q, G.W. Nl, J.I. Prer,S.C. Shuer, ad C. Shleper. 2006. Arhaea predmae amgamma-xdzg prkarye l. Naure (Ld) 442:806809.

Lek, R.E. 1997. Te f a reaeFrm he perpeve fa aerum. Ca Fud. Symp. 207:131140.

Lek-Hupkv, M., J. Blahv, V. Krmry, Sr., ad K. Krlkv. 1996.Mlza f a reae fr rafer Pseudomonasaeruginosa. J. Chemher. 8:261265.

Levy, M.S., E. Balder, ad R. Nagel. 1993. Effe f mua SOSgee UV-dued pree ex fTn10 Escherichia coli. Mua.Re. 293:241247.

Levy, S.B., ad R.V. Mller. 1989. Gee rafer he evrme. Evr.Behl. Ser. MGraw-Hll, New Yrk.

Leer, C.A., R.M. Hall, ad A.O. Summer. 1999. rap Tn21, flaghpf he flag geme. Mrl. Ml. Bl. Rev. 63:507522.

Llley, A., ad M. Baley. 1997. Te aqu f dgeu plamd y ageeally marked peudmad ppula lzg he ugar eephyphere relaed lal evrmeal d. Appl. Evr.Mrl. 63:15771583.

Lvek ad Pulry Evrmeal Sewardhp. 2005. Appedx C:Lvek ad pulry maure haraerza. Avalale a hp://www.lpe.rg/Le/Le21/21_9_maure_haraer.pdf (verfied 16Fe. 2009).

Lke, M.-L., J. jrelud, ad B. Hallg-Sree. 2002. Deermaf he dru effi e (lgKd) f xyerayle, yl A,laqudx ad merdazle maure. Chemphere 48:351361.

Lrez, M.G., ad W. Wakeragel. 1987. Adrp f DNA ad advarale degrada rae f adred DNA. Appl. Evr. Mrl.53:29482952.

Lrez, M.G., ad W. Wakeragel. 1994. Baeral gee rafer y auralgee rafrma he evrme. Mrl. Rev. 58:563602.

Lvelad, J.P., S. Bhaaharjee, J.N. Rya, ad M. Elmeleh. 2003. Clldrapr a gehemally heergeeu pru medum: Aquferak experme ad mdelg. J. Cam. Hydrl. 65:161182.

Lu, A., J. Zhu, ad P.M. Ndegwa. 2002. Ifluee f aaer pre-

dg phphru remval we maure y aera.Waer Ar Sl Pllu. 140:219230.Lu, N., S. Perera, O. Sah, J. L, S. Huag, L. Mhel, ad Q. Zhag. 2005.

Ehaed in vivo fie f flurqule-rea Campylobacterjejuni he aee f a ele preure. Pr. Nal. Aad.S. USA 102:541546.

MaDald, J.M. 2008. Te em rgaza f U.S. rlerprdu. E. Ifrma Bull. 38. Avalale a hp:www.er.uda.gv/pula/e38/e38.pdf (verfied 19 Fe. 2009). USDA ERS,

Wahg, DC.

Maler, B.A. 1995. Develpg a aal drkg waer regula frdfe f grudwaer. Grud Waer M. Rem. 15:7784.

Malk, A., E.-K. elk, C. Bh, U. Bkelma, K. Kel, ad E.Grhma. 2008. Dee f jugave plamd ad areae gee arpge l frm Germay ad Ida. FEMSMrl. Le. 279:207216.

Maher, J.J., S.R. Clarke, D. Hauma, P. llma, V.R. Beg, ad S.K.Grd. 2004. Ih f reae plamd rafer Escherichiacoli y phre, hlrerayle, ara, ad phre/amral ma. Ava D. 48:317323.

Mazder, P., ad J. Dave. 1991. Gee rafer ewee daly relaedaera. Au. Rev. Gee. 25:147171.

MKay, L.D., J.A. Cherry, ad R.W. Gllham. 1993. Feld experme afraured lay ll. 1. Hydraul duvy ad fraure aperure. WaerReur. Re. 29:11491162.

MMurry, S.W., M.S. Cye, ad E. Perfe. 1998. Feal lfrm raprhrugh a l lk ameded wh pulry maure. J. Evr.Qual. 27:8692.

Mller, R.V. 2001. Evrmeal aerphage-h era: Far

ru aural radu. Ae va Leeuwehek79:141147.

Mg, L.-J. 2003. Sruure ad fu f mealla. Med. Re.Rev. 23:697762.

Mherlh, E., ad E.H. Marh. 1984. Mral urvval he evrme:Baera ad rkeae mpra huma ad amal healh. Sprger-Verlag, New Yrk.

Myaz, K., M. ujmura, Y. Kawaraaya, ad M. akura. 2007. Cryalruure f a arhaeal hmlgue f muldrug reae reprerpre, EmrR, frm hyperhermphl arhaea Sulfolobus tokodaiira: VII. Pre ruure, fu. Bfrma 67:11381146.

Naer, A.M., ad S.D. Oma. 1999. Quaave aeme f heava f pahge ad dar vrue aural waer ure.

Waer Re. 33:17481772.

Naer, A.M., Y. hry, ad B. Faal. 1993. Cmparave urvval fE. coli,F+ aerphage, HAV ad plvru 1 waewaer ad grudwaer.

Waer S. ehl. 27:401407.Neraka Beef Cul. 2007.Beef dury frma, Sae/dury fa.

Avalale hp:/eeef.rg/ae_dury_fa.ap (verfied 16 Fe.2009). Neraka Beef Cul, .

Nele, K.M., K. Smalla, ad J.D. va Ela. 2000. Naural rafrmafAcinetobacterp. ra BD413 wh ell lyae fAcinetobacterp.,Pseudomonas fluorescens, ad Burkholderia cepacia l mrm.

Appl. Evr. Mrl. 66:206212.Nele, K.M., ad J.D. va Ela. 2001. Smulary effe f mpud

pree he rhzphere aural rafrma fAcinetobacterp.BD413 l. Sl Bl. Bhem. 33:345357.

Nklakpulu, .L., S. Ega, L.S. va Overeek, G. Gullaume, H. Heuer,E.M.H. Wellg, J.D. va Ela, J.-M. Cllard, K. Smalla, ad A.D.Karagu. 2005. PCR dee f xyerayle reae geeotr(A) ad otr(B) erayle-rea repmyee lae frmdvere haa. Curr. Mrl. 51:211216.

Nker, A., M. Burr, ad A.K. Camper. 2007. Geyp mral mmuyprfilg: A ral ehal revew. Mr. El. 54:276289.

OCr, S., ad D.S. Aga. 2007. Aaly f erayle a l: Advae exra, lea-up, ad quafia. red Aal.Chem. 26:456465.

ODell, J.D., M.E. Eg, ad D.D. Hward. 1995. Surfae applaf lqud we maure: Chemal varaly. Cmmu. Sl S. Pla

Aal. 26:31133120.

Ogram, A., G.S. Sayler, D. Gu, ad R.J. Lew. 1988. DNA adrp l ad edme. Evr. S. ehl. 22:982984.

Oguea, O., G. Sayler, ad R. Mller. 1992. Appla f DNA pre

aaly f aerphage dru paer he evrme. Appl.Evr. Mrl. 58:20462052.

Ohle, K., . ere, G. Werer, U. Waller, D. Lffl er, W. Zeuhr, W. We, ad J. Haker. 2003. Impa f a jugaalreae gee rafer Staphylococcus aureus ewage. Evr.Mrl. 5:711716.

Olva, Y., ad B.R. Faulker. 2008. Feal ure rakg y areae a aly a waerhed exhg lw reae. Evr.M. Ae. 139:1525.

Oa, L.J., ad .M. LaPara. 2003. yl-rea aera ulvaed frmagrulural l. FEMS Mrl. Le. 220:1520.

Oerlad, M., J. Leevu, . Leevu, H. Jarve, L. Pyy, J. evu, ad P.Huve. 1995. Amral ad merury reae aer gram-egave all feal flra amg per wh ad whu dealamalgam fillg. Amr. Age Chemher. 39:24992502.

Paee, J., W. Cyper, K. Pauwel, E. Re, ad J. Hgmare. 1995. Sudyf he aly f yl A aqueu lu. J. Pharm. Bmed.

Aal. 13:11531159.Page, E., L.J. Mrzer, ad P. Sme. 1992. Adrp f DNA lay

meral: Pre aga DNaeI ad fluee gee rafer.FEMS Mrl. Le. 97:3139.

Park, N., .N. Bladfrd, Y.-S. Wu, ad P.S. Huyakr. 1994. CANVAS:A mpe aalyal-umeral mdel fr vral ad lue raprmula, ver 2.0. HydrGeLg, I., Herd, VA.

Park, H., ad Y.-K. Chug. 2007. Degrada f a (erayle,ulfahazle, ampll) ug ezyme f Gluah S-raferae.Hum. El. Rk Ae. 13:11471155.

Parvee, S., J. Lukak, .M. S, M.L. ampl, K.M. Prer, S. Shepard,K. Brau, ad S.R. Farrah. 2006. Gegraphal vara a

8/3/2019 Ind 44197785

22/23


reae prfile fEscherichia colilaed frm we, pulry, eef addary ale farm waer ree pd Flrda. J. Appl. Mrl.100:5057.

Paer, A.J., R. Clagel, P. Spgagla, ad K.P. S. 2007. Dru fpefi erayle ad erhrmy reae gee evrmealample aeed y mararray dee. Evr. Mrl. 9:703715.

Payme, P., ad R. Arm. 1989. Vru remval y drkg waer reamepree. Cr. Rev. Evr. Cr. 19:1531.

Plla, S.D., K.W. Wdmer, K.G. Marwk, ad S.C. Rke. 1997.A reae prfile fEscherichia colilaed frm rural adura evrme. J. Evr. S. Healh A 32:16651675.

Pk, L.A., W.F. Hl, ad F.E. All. 1961a. A l: 1. Phy-hemal ude f a-lay mplexe. Sl S. 91:2228.

Pk, L.A., D.A. Sulde, ad F.E. All. 1961. A l: II.Exe ad meham f releae. Sl S. 91:9499.

Pk, L.A., D.A. Sulde, ad F.E. All. 1962. A l: 4.Plypepde ad marlde. Sl S. 94:121131.

Pwell, K.L., R.G. aylr, A.A. Cr, M.H. Barre, S. Pedley, J. Sellwd,S.A. rwdale, ad D.N. Lerer. 2003. Mral ama f wura ade aqufer he UK. Waer Re. 37:339352.

Pre, L.M., J.P. Harley, ad D.A. Kle. 1999. Amral hemherapy.p. 678696. In Mrlgy. 4h ed. MGraw-Hll, New Yrk.

Ralle, M., ad N.H. Spld. 2000. Srp ad mly f merdazle,laqudx, xyerayle, ad yl l. Chemphere 40:715722.

Ramadha, A.A., ad E. Hegedu. 2005. Survvaly f vamy reaeer ad fie f vamy reae aqu. J. Cl.Pahl. 58:744746.

Rere, G., C. Pard, P. Nrmad, ad P. Sme. 1993. Ke f heperee f hrmmal DNA frm geeally egeeredEscherichiacolirdued l. Appl. Evr. Mrl. 59:42894294.

Rher, B.., M.D. kah, R.D. Gdad, ad J.L. Nele. 1995. Aegprduer awaree f he mpa f we prdu he evrme.

J. f Exe 33(4). Avalale a hp://www.je.rg/je/1995augu/r4.hml (verfied 16 Fe. 2009). Kaa Sae Uv., Mahaa.

Reefeld, C.S., R.M. Gdma, ad J. Hadelma. 2004. Uuluredl aera are a reervr f ew a reae gee. Evr.Mrl. 6:981989.

Rer, M.C. 1998. A reae meham aera f ral adupper reprary rg. I. J. Amr. Age 9:255267.

Rer, J.B., ad S.C. Ederg. 1997. Naural pre f prgad well drkg waer aga urfae mral ama. I.Hydrgelgal parameer. Cr. Rev. Mrl. 23:143178.

Rll, D.M., ad R.R. Clwell. 1986. Vale u ulurale age

f Campylobacter jejuniad rle urvval he aural aquaevrme. Appl. Evr. Mrl. 52:531538.

Rmawk, G., M. Lrez, ad W. Wakeragel. 1993. Ue f plymeraeha rea ad elerpra f Escherichia coli mr heperee f exraellular plamd DNA rdued aural l.

Appl. Evr. Mrl. 59:34383446.Rz, C.A. 2004. Maageme redue rge le amal prdu.

J. Am. S. 82 (E. uppl.):E119E137.Sa, R., L.J. Halver, ad J.C. Lrmr. 2003. Rafall mg ad

frequey fluee leahg f Escherichia coliRS2G hrugh lfllwg maure appla. J. Evr. Qual. 32:18651872.

Salyer, A.A., ad C.F. Amle-Cueva. 1997. Why are a reae gee rea elma? Amr. Age Chemher. 41:23212325.

Salyer, A.A., A. Gupa, ad Y. Wag. 2004. Huma eal aera areervr fr a reae gee. red Mrl. 12:412416.

Salyer, A.A., N.B. Shemaker, A.M. Seve, ad L.Y. L. 1995. Cjugave

rap: A uuual ad dvere e f egraed gee rafereleme. Mrl. Rev. 59:579590.

Samuele, O.B., B.. Luead, A. Ervk, ad S. Fjelde. 1994. Saly faaeral age a arfial mare aquaulure edme udeduder larary d. Aquaulure 126:283290.

Saderma, H.J. 1992. Pla mealm f xe. red Bhem.S. 17:8284.

Sa Dmg, J.W., S. Harm, ad J. Bee. 2000. Survval fSalmonellapee rver waer. Curr. Mrl. 40:409417.

Sapka, A.R., F.C. Currer, K.E. G, ad K.J. Shwa. 2007. A-rea eer ad feal dar urfae waer ad grudwaermpaed y a eraed we feedg pera. Evr. Healh

Perpe. 115:10401045.Sarmah, A.K., M.. Meyer, ad A.B.A. Bxall. 2006. A glal perpeve

he ue, ale, expure pahway, urree, fae ad effe f veerarya (Va) he evrme. Chemphere 65:725759.

Sayah, R.S., J.B. Kaeee, Y. Jh, ad R. Mller. 2005. Paer famral reae erved Escherichia coli lae aedfrm dme- ad wld-amal feal ample, huma epage, adurfae waer. Appl. Evr. Mrl. 71:13941404.

Sadura, J.E., ad M.D. Sey. 1997. Vral ad aeral ama fgrudwaer frm -e ewage reame yem. Waer S. ehl.35:107114.

Shklmaer, P., ad H. Shmeger. 1995. Frequey f geeralzed radugphage aural lae f he Salmonella typhimurium mplex. Appl.Evr. Mrl. 61:16371640.

Shjve, J.F., ad S.M. Haazadeh. 2000. Remval f vrue y lpaage: Overvew f mdelg, pree, ad parameer. CRC Cr.Rev. Evr. S. ehl. 30:49127.

Shm, H., H. Haapakaga, ad P. va Beele. 2005. Effe f a l mrrgam: me ad ure fluee pllu-duedmmuy lerae. Sl Bl. Bhem. 37:18821892.

Shm, M.A., S.D. Eva, ad G.W. Radall. 1995. Effe f lqud maureappla mehd l rge ad r gra yeld. J. Prd.

Agr. 8:186189.

Segelv, G., Y. Ager, B. Hallg-Sre, S.B. Balda, J.S. Ader, ad L.B.Jee. 2003. Baeral a reae level Dah farmlad a areul f reame wh pg maure lurry. Evr. I. 28:587595.

Sve, N.A., D. Kallfida, K. Smalla, J.D. va Ela, J.-M. Cllard, A.D. Karagu,

ad E.M.H. Wellg. 2002. Ourree ad reervr f areae gee he evrme. Rev. Med. Mrl. 13:1528.

Shea, K.M. 2004. Nherapeu ue f amral age amalagrulure: Impla fr pedar. Pedar 114:862868.

Shemaker, N.B., H. Vlamak, K. Haye, ad A.A. Salyer. 2001. Evdeefr exeve reae gee rafer amg Bacteroidespp. ad amgBacteroides ad her geera he huma l. Appl. Evr.Mrl. 67:561568.

Shwh, S.A., ad R.E. Adrew, Jr. 1992. erayle ehae Tn916-medaed jugal rafer. Plamd 28:213224.

Shyu, J.B.H., D.P. Le, ad D.K. Newma. 2002. Preve rle f tolC effl ux f he eler hule ahraque-2,6-dulfae. J. Baerl .184:18061810.

Smp, J.M., J.W. Sa Dmg, ad D.J. Reaer. 2002. Mral urerakg: Sae f he ee. Evr. S. ehl. 36:52795288.

Sm, J.D. 1993. Flw ad rapr hrugh fraured lay ll: A larary udy.

M.S. he. Dep. f Earh See, Uv. f Waerl, Waerl, ON.Smuek, J., M. Seja, ad M.. va Geuhe. 1999. Te HYDRUS-2D

fware pakage fr mulag he w-dmeal mveme fwaer, hea, ad mulple lue varaly-auraed meda, Ver2.0. U.S. Saly La., U.S. Agr. Re. Serv., Rverde, CA.

Shle, B.B., ad R.D. Guy. 1987a. Mdel fr erayle aquaevrme. I. Iera wh ee lay yem. Waer Ar SlPllu. 32:303314.

Shle, B.B., ad R.D. Guy. 1987. Mdel fr erayle aquaevrme. II. Iera wh hum uae. Waer Ar SlPllu. 32:315321.

Skld, O. 2000. Sulfamde reae: Meham ad red. Drug Re.Upda. 3:155160.

Smh, D.H. 1967. R far medae reae merury, kel ad al.See (Wahg, DC) 156:11141116.

Smh, M.S., R.K. Yag, C.W. Kapp, Y. Nu, N. Peak, M.M. Hafel,J.C. Gallad, ad D.W. Graham. 2004. Quafia f eraylereae gee feedl lag y real-me PCR. Appl. Evr.Mrl. 70:73727377.

Sey, M.D., L.A. Kha, V.R. Hll, E. Allja, ad S. Plla. 2001. Pahge amal wae ad he mpa f wae maageme prae herurvval, rapr ad fae. Whe Paper Summare. Avalale lehp://www.al.u.edu/wae_mg/aleer/whepaperummare/pahge.pdf (verfied 16 Fe. 2009).

Slm, J.M., R. Magu, A. Srvaava, ad A.D. Grma. 1995.Cverge eg pahway medae repe w exraellularmpeee far Bacillus subtilis. Gee Dev. 9:547558.

Srum, H., ad .M. LAe-Lud. 2002. A reae fd-relaedaeraA reul f erferg wh he glal we f aeral gee.

8/3/2019 Ind 44197785

23/23

I. J. Fd Mrl. 78:4356.Srum, H., ad M. Sude. 2001. Reae a he rmal flra

f amal. Ve. Re. 32:227241.Sam, A.J.M., F.A.M. de Bk, C.M. Plugge, M.H.A. va Eeker, J. Dlfig,

ad G. Shraa. 2006. Exellular eler rafer aaer mralmmue. Evr. Mrl. 8:371382.

Sa, .B. 2007. Prphage-lke gee rafer age-vel mehamf gee exhage fr Methanococcus, Desulfovibrio, Brachyspira, adRhodobacterpee. Aaere 13:4349.

Sa, .B., ad S.B. Humphrey. 2003. Ila f erayle-rea

Megasphaera elsdeniira wh vel ma gee ma ftet(O)ad tet(W) frm we. Appl. Evr. Mrl. 69:38743882.Sa, .B., S.B. Humphrey, K.P. S, ad H.J. Fl. 2005. Hyrd tet

gee ad tet gee melaure: Reque fr p. Amr.Age Chemher. 49:12651266.

Sa, .B., J.S. MDwall, ad M.A. Ramue. 2004. Dvere eraylereae geype f Megasphaera elsdeniira elevely uluredfrm we fee. Appl. Evr. Mrl. 70:37543757.

Seve, A.M., N.B. Shemaker, L.Y. L, ad A.A. Salyer. 1993. erayleregula f gee Bacteroidesjugave rap. J. Baerl.175:61346141.

Sewar, G.J. 1989. Te meham f aural rafrma. p. 139164.In S.B. Levy ad R.V. Mller (ed.) Gee rafer he evrme.MGraw-Hll, New Yrk.

Sddard, C.S., M.S. Cye, ad J.H. Grve. 1998. Feal aeral urvvalad filra hrugh a hallw agrulural l: mg ad llageeffe. J. Evr. Qual. 27:15161523.

Szky, G. 2000. Peree ad lgal avy l f edalpre frm Bacillus thuringiensisad f aeral DNA ud layad hum ad. J. Evr. Qual. 29:691705.

auxe, R.V. 1997. Evlvg fdre deae: A evlvg pul healhhallege. Emerg. Ife. D. 3:425434.

mey, J.F., J. Pr, J. Gle, ad J. Spaer. 1978. Heavy-meal ad areae he aeral flra f edme f New Yrk Bgh. Appl.Evr. Mrl. 36:465472.

ll, J. 2001. Srp f veerary pharmaeual l: A revew.Evr. S. ehl. 35:33973406.

rre, O.R., R.Z. Krma, S.A. Zahler, ad G.M. Duy. 1991. Tejugave rap Tn925: Ehaeme f jugal rafer yerayle Enterococcus faecalisad mlza f hrmmal gee Bacillus subtilisad E. faecalis. Ml. Ge. Gee. 225:395400.

revr, J.. 1999. Evlu f gee rafer aera. Wrld J. Mrl.Behl. 15:16.

U, A., ad M.J. G. 2003. Mveme f faeal aera hrugh he vadeze. Waer Ar Sl Pllu. 149:327337.

U f Cered Se. 2001. Hggg : Emae f amralaue lvek. p. 109. UCS Pul., Camrdge, MA.

USDA. 2001a. Par I: Referee f we healh ad maageme heUed Sae, 2000, Naal Amal Healh Mrg Syem. N.N338.0801. USDA, Fr Cll, CO.

USDA. 2001. Par II: Referee f we healh ad maageme heUed Sae, 2000, Naal Amal Healh Mrg Syem. N.N355.0202. USDA, Fr Cll, CO.

USDA. 2007. Swe 2006, Par II: Referee f we healh ad healhmaageme prae he Ued Sae, 2006 USDA:APHIS:VS,CEAH. N. N479.1207. USDA, Fr Cll, CO.

USDA NASS. 2002. Sa f ale, hg, ad heep. Avalale a hp://www.a.uda.gv/Pula/Ag_Sa/2008/Chap07.pdf(verfied 16 Fe. 2009).

USDA NRCS. 1995. Amal maure maageme. NRCS/RCA ue ref 7,De. 1995. Avalale a hp://r.uda.gv/ (verfied 16 Fe. 2009(.

USGAO. 1999. Te agrulural ue f a ad mpla frhuma healh. Geeral Aug Offi e. Pul. GAO-RCED 9974.U.S. Geeral Aug Offi e, Wahg, DC.

Uah Deparme f Healh. 2007. Meda dpal ummary repr. Avalale a hp://healh.uah.gv/prerp/pdf/NewHamphre_Dpal_ehal.pdf (verfied 16 Fe. 2009).

Valee, P.J., N.B. Shemaker, ad A.A. Salyer. 1988. Mlza fBacteroides plamd y Bacteroides jugal eleme. J. Baerl.

170:13191324.va Ela, J.D., B.B. MSpadde Gardeer, A.C. Wler, ad E. Sm. 1998.

Ila, haraerza, ad rafer f ryp gee-mlzgplamd he whea rhzphere. Appl. Evr. Mrl.64:880889.

Vlkhv, D., V. Chzhkv, K. Chumakv, ad A. Raly. 2003. Mrarrayaaly f eryhrmy reae deerma. J. Appl. Mrl.95:787798.

Wager, M., H. Smd, A. Ly, ad J. Zhu. 2007. Uravellg mralmmue wh DNA-mrarray: Challege ad fuure dre.Mr. El. 53:498506.

Wag, G., ad M.P. Dyle. 1998. Survval f eerhemrrhag Escherichiacoli0157:H7 waer. J. Fd Pr. 61:662667.

Wag, R.-F., W.-W. Ca, ad C.E. Cergla. 1996. PCR dee adquaa f predma aaer aera huma ad amalfeal ample. Appl. Evr. Mrl. 62:12421247.

We, V., ad J. Dave. 1993. A prepara a DNA: Aure f drug reae gee? Amr. Age Chemher.37:23792384.

Weauer, M.G., ad F. Raulzadega. 2004. Are vrue drvg mraldverfia ad dvery? Evr. Mrl. 6:111.

Wellg, F.M., A.L. Lew, ad C.W. Mua. 1974. Vru urvval fllwgwaewaer pray rrga f ady l. In J.F. Mala ad B.P. Saek(ed.) Vru urvval waer ad waewaer yem. Uv. f exa a

Au, Au, X.

Wellg, F.M., A.L. Lew, C.W. Mua, ad L.V. Pere. 1975.Demra f vru grudwaer afer effl ue dharge l.

Appl. Mrl. 29:751757.Wellg, E.M., N. Crewell, ad P.R. Herr. 1992. Gee rafer ewee

repmyee l. Gee 115:193198.

Whle, G., N.B. Shemaker, ad A.A. Salyer. 2002. Idefia f wgee vlved he mdula f jugal rafer f he Bacteroidesjugave rap CDO. J. Baerl. 184:38393847.

Wgg, B.A., R.W. Adrew, R.A. Cway, C.L. Crr, E.J. Draz, D.P.Dughery, J.R. Eppard, S.R. Kupp, M.C. Lmj, J.M. Meeerg,

J.M. Rehar, J. S, R.L. rrj, ad M.E. Zmmerma. 1999.Ue f a reae defy p ure f feal pllu.

Appl. Evr. Mrl. 65:34833486.

Wllam, K.E., M. Radevh, D.W. Smh, ad K.E. Wmmak. 2007.Idee f lygey wh emperae ad exreme l evrme.Evr. Mrl. 9:25632574.

Wllam, K.E., M. Radevh, ad K.E. Wmmak. 2005. Audaead dvery f vrue x Delaware l. Appl. Evr. Mrl.

71:31193125.Wegerauer, M., H. Lagler, W. Grager, ad H. Burgma. 2005. DNA a prepara: Aee f a reae gee. Amr.

Age Chemher. 49:24902494.

Wmmak, K.E., ad R.R. Clwell. 2000. Vrplak: Vrue aquaeyem. Mrl. Ml. Bl. Rev. 64:69114.

Yag, S., ad K. Carl. 2003. Evlu f a urree arver hrugh pre, ura, ad agrulural ladape. Waer Re.37:46454656.

Yae, M.V., ad W.A. Jury. 1995. O he ue f vru rapr mdelg frdeermg regulary mplae. J. Evr. Qual. 24:10511055.

Yae, M.V., W.A. Jury, S.R. Yae, D.L. Ader, L.M. Sark, ad P. Sherlm.2000. Meaureme f vru ad dar urvval ad rapr he uurfae. Prje 262. Amera Waer Wrk Re. Fuda,Dever, CO.

Yae, M.V., ad S.R. Yae. 1988. Mdelg mral fae he uurfaeevrme. Cr. Rev. Evr. Crl 17:307344.

Yu, Z., F.C. Mhel, G. Hae, . Wum, ad M. Mrr. 2005.Develpme ad appla f real-me PCR aay fr quafiaf gee edg erayle reae. Appl. Evr. Mrl.71:69266933.

Zha, Z., M.P. Dyle, J. Shere, ad L. Garer. 1995. Prevalee feerhemrrhag Escherichia coli0157:H7 a urvey f dary herd.

Appl. Evr. Mrl. 61:12901293.

Zlke, L.M., ad R.W. Weaver. 1978. Effe f evrmeal far urvval fSalmonella typhimurium l. J. Evr. Qual. 7:593597.

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