Short communication

The effects of feeding broiler litter on microbial contamination ofbeef carcasses

Jesse R. Davis 1, Jason K. Apple *, Dianne H. Hellwig, Elizabeth B. Kegley,Fred W. Pohlman

Department of Animal Science, B103C AFLS Administration Bldg, University of Arkansas, Fayetteville, AR 72701, USA

Received 19 November 2001; received in revised form 11 January 2002; accepted 2 February 2002

Abstract

Two experiments were conducted to test the effects of feeding broiler litter, either directly in the diet or indirectly through

pasture-fertilization, to beef cattle on the incidence of Salmonella typhimurium (S) and Escherichia coli O157:H7 (EC) contamination

of carcasses and ground beef. In Experiment 1, beef cows (n ¼ 32) were allotted either ad libitum access to grass hay or a formulateddiet (80% deep-stacked broiler litter and 20% corn). In Experiment 2, beef cows (n ¼ 32) were assigned to graze on pastures fertilizedwith a commercial fertilizer or fresh broiler litter. Cows in Experiment 1 were harvested following a 56-d feeding period; whereas,

cows in Experiment 2 were harvested after 5, 10, 20, and 40 d of grazing pastures. All samples of muscle, purge, and ground beef

were culture-negative for S and EC, suggesting that beef cattle may consume properly handled deep-stacked broiler litter, or

pastures fertilized with fresh litter, without increasing the likelihood of carcass/meat contamination with S and (or) EC. � 2002

Elsevier Science Ltd. All rights reserved.

Keywords: Broiler litter; Beef carcasses; Salmonella typhimurium; E. coli O157:H7

1. Introduction

Broiler litter is an abundant bioresource often pro-duced on small farms in many parts of the USA, anddisposal of this byproduct may be problematic. Deep-stacked broiler litter has long been fed to cattle. As earlyas 1955, Noland et al. (1955) showed that ruminantanimal performance and health could be maintained byfeeding diets formulated with large quantities of broilerlitter. However, the nutritional characteristics of broilerlitter, especially low energy content (Rankins and Rude,1996), reduced digestibility (Goetsch and Patil, 1993),and high copper content (Bagley et al., 1996), limit itsinclusion in ruminant diets. Therefore, the most preva-lent method of litter disposal is as a fertilizer because ofits organic nitrogen content (Nicholson et al., 1999).Although fresh broiler litter is rarely fed directly to

cattle, cattle may indirectly consume fresh litter while

grazing pastures fertilized with fresh litter or drinkingfrom ponds contaminated by run-off from litter-fertil-ized pastures. Fresh broiler litter may harbor a varietyof potentially pathogenic bacteria, including: Clostri-dium, Salmonella, Staphylococcus, Streptococcus, Esche-richia coli, Yersinia, Listeria, and Campylobacter species(Schefferle, 1965; McCaskey and Anthony, 1979; Kelleyet al., 1994, 1995). However, the practice of ‘‘deep-stacking’’ broiler litter has been shown to effectivelyreduce E. coli, Aeromonas hydrophila, Pseudomonas aeru-ginosa, Yersinia enterocolitica, Salmonella spp., andCampylobacter jejuni to levels well below the detectionlimit of 30 CFU/g dry matter (Kelley et al., 1995). Deep-stacking broiler litter results in elevated temperatures(54–66 �C; McCaskey and Harris, 1982) and high am-monia accumulation (Gates et al., 1998), which, actingin concert, produces an environment unsuitable for bac-terial survival.Public concern about the practice of feeding broiler

litter was aroused by a popular press report (Satchelland Hedges, 1997) that implied a linkage between theincidence of E. coli O157:H7 in ground beef, as well asother food-borne outbreaks, to cattle consuming broilerlitter. However, very little, if any, scientific information

Bioresource Technology 84 (2002) 191–196

*Corresponding author. Tel.: +1-479-575-4840; fax: +1-479-575-

7294.

E-mail address: japple@uark.edu (J.K. Apple).1 Present address: Department of Animal Sciences and Industry,

Kansas State University, Weber Hall, Manhattan, KS 66502-0201.

0960-8524/02/$ - see front matter � 2002 Elsevier Science Ltd. All rights reserved.

PII: S0960-8524 (02 )00037-8

exists that could be used to confirm or contradict theseclaims. Therefore, the objective of this study was todetermine whether feeding broiler litter to beef cattle,either directly in the diet or indirectly through fertiliza-tion, affected the incidence of E. coli O157:H7 (EC) andSalmonella typhimurium (S) found on beef carcasses,beef trimmings, and in ground beef.

2. Methods

Mature (6–8 years of age), crossbred cows (n ¼ 65)were culled from the breeding herd at the University ofArkansas Southwest Research and Extension Center atHope, and transported to the University of ArkansasBeef Research Unit, at Savoy, approximately threemonths before the onset of trial initiation to acclimatethe cows to the environment. Cows were divided intotwo groups upon arrival, and placed on separate pas-tures for ease of movement. The first group of cows(n ¼ 33) was assigned to Experiment 1, which beganJanuary 26, 1998, and the second group of cows (n ¼ 32)was assigned to Experiment 2, which began on April 23,1998.

2.1. Experiment 1

Approximately 13.6 metric tons of broiler litter waspurchased from a local producer who cooperated fullywith all sampling requirements prior to bird removal.The bedding material was predominantly pine shavings,and six sequential broiler-growing periods had beenconducted before this litter cleanout, with no additionalbedding applied between growing periods. Cloacalswabs were taken from 50 randomly selected birds priorto removal, and five floor-drag swabs were taken fromthe broiler house immediately following bird removal.Cloacal and floor-drag swabs were subsequently ana-lyzed for presence of EC and S. Packed litter was re-moved and transported to the University of ArkansasBeef Cattle Unit. Upon arrival, broiler litter was stackedto a depth of 1.5 m as prescribed in the Arkansas Co-operative Extension Publication ‘‘Feeding Broiler Litterto Beef Cattle’’ (Davis, 1995). Immediately after deep-stacking, temperature probes were inserted across thestack in order to monitor temperatures both deep in-side the stack and near the surface. Furthermore, sam-ples of litter, as well as samples of hay, were collectedand analyzed for nitrogen (to determine crude proteincontent of each feedstuff; AOAC, 1984), dry matter, ash(AOAC, 1984), and neutral detergent fiber (filter bagtechnique; ANKOM Technology, Fairport, NY) inorder to formulate treatment diets.Thirty three mature, crossbred beef cows were

weighed 15 d before beginning the trial, and one cowwas excluded from the trial due to excessive body

weight. The remaining 32 cows were then assignedrandomly to ad-libitum access to either: (1) a diet con-sisting of 80% deep-stacked broiler litter and 20% corn,supplemented with 0.91 kg long-stem grass hay/cow/d;or (2) long-stem grass hay. The grass hay fed to cowswas from pastures fertilized with only a commerciallyavailable chemical fertilizer. Diets were formulated tobe approximately isocaloric, and crude protein contentmet, or exceeded, the requirements for non-pregnant,aged, beef cows (National Research Council, 1996). Allcows had ad libitum access to water, and cows fed thehay-diet were supplied with free-choice block mineral;whereas, due to the high mineral content of deep-stacked litter, cows consuming the litter-diet weresupplied with white block salt. Furthermore, at thebeginning of the trial, all cows were given a 4-ml sub-cutaneous injection of supplemental vitamins contain-ing 500,000 IU/ml of vitamin A and 75,000 IU/ml ofvitamin D.Fourteen days before introduction of dietary treat-

ments, cows were weighed, again, and rectal-palpated‘‘grab’’ samples of feces were collected and cultured forthe presence of S and EC. Subsequently, cows were as-signed to pens of four cows each, and a single pen waskept empty between each pen of cows to insure no fence-line contact between cows at all times. Fecal sampleswere taken from each cow seven days before, and on themorning of diet introduction. On 7, 14, 21, 28, 35, 42,49, and 56 d of the feeding trial, fecal samples werecollected from each cow and analyzed for the presenceof S and EC. At the conclusion of the 56-d feeding pe-riod, all cows were transported approximately 26 km tothe University of Arkansas Red Meat Abattoir. Cowsreceiving the hay-only diet were harvested first. Thetrailer and all harvest facilities and equipment werecleaned with a commercially available detergent (Ecol-abs, St. Paul, MN) and hot (79 �C) water, and sanitizedwith a solution containing 8.4% chlorine (Ecolabs, St.Paul, MN) before transport and harvest of cows re-ceiving the broiler-litter diet treatment.

2.2. Experiment 2

Culled mature, crossbred beef cows (n ¼ 32) wereweighed and allotted randomly to: (1) graze one of four0.455-square hectare grass pastures fertilized with freshbroiler litter; or (2) graze one of four 0.455-squarehectare grass pastures fertilized with a commerciallyavailable inorganic fertilizer. Fecal grab samples wereobtained for microbial analyses from all cows 14 and 7 dbefore, as well as on the morning (designated d-0) whencows were introduced to the treated pastures. Again,cows were afforded ad libitum access to water and free-choice block mineral, and received a 4-ml injection ofsupplemental vitamins A and D.

192 J.R. Davis et al. / Bioresource Technology 84 (2002) 191–196

Fresh broiler litter was purchased from a local pro-ducer, and transported immediately after cleanout to theUniversity of Arkansas Beef Research Unit. Fresh litterwas surface applied to the four experimental pastures ata rate of 4.48 metric tons/hectare. During litter appli-cation, four random samples of fresh litter were col-lected and analyzed for the presence/absence of S andEC. Immediately following pasture fertilization, cowswere placed into their respective treatment pastures. Anempty 0.455-square hectare pasture was maintainedbetween each treatment pasture to avoid fence-line con-tact between cows of different treatments. On the des-ignated days preceding harvest (4, 9, 19, and 39 d ofthe grazing period), cows were weighed and fecal sam-ples were collected and cultured for the presence of Sand EC. On 5, 10, 20, and 40 d, one cow from eachpasture was transported approximately 26 km to theUniversity of Arkansas Red Meat Abattoir, renderedunconscious and insensitive to pain by captive-boltstunning and harvested according to industry-acceptableprocedures. Cows grazing the chemically fertilized pas-tures were harvested first. To reduce the chance of cross-contamination between treatment groups, all equipmentand facilities, as well as the trailer, were cleaned andsanitized before cows grazing the litter-fertilized pas-tures were transported and harvested.

2.3. Postmortem sample collection

Following standard dressing procedures, carcasseswere split down the vertebral column, and both sideswere thoroughly washed with cool (8 �C) water. Theleft side of each carcass received a 2% lactic acid rinseto simulate a post-harvest sanitation step possibly em-ployed by small-scale meat processors. Muscle and fatsamples from the neck and bung areas (incision samples)of the carcass were taken from both sides, placed inindividually identified Whirl-Pak� bags, and immedi-ately cultured for S and EC. Approximately 10 kg ofpre-rigor beef trimmings from the external surfaces ofthe round, loin, rib, chuck, flank, plate and brisket wereremoved from each side, packaged in individual ‘‘mini-combos’’ (sterile plastic liner bag housed in a wax-coated, corrugated box), and refrigerated at 2 �C.After 6 d of refrigerated storage, samples of purge

(moisture that collects in the bottom of packages ofmeat) were collected for microbial analyses, and trim-mings were then ground twice through a Hobart grinder(model 310; Hobart, Troy, OH) with a 3.2-mm plate. Allparts and equipment were washed with hot (79 �C)water and commercially available detergent (Ecolabs,St. Paul, MN), and sanitized with a 4% chlorine solutionbetween sample grindings. Random samples of groundbeef, as well as purge samples, were subsequently cul-tured for the presence of S and EC.

2.4. E. coli O157:H7 isolation

The isolation of E. coli O157:H7 from fecal, purge,and meat samples followed the procedures outlined byHitchins et al. (1998). Approximately 25 g of meat (ei-ther neck and bung incision samples or ground beef)were placed in Stomacher� bags (Seward, London, UK)with 225 ml of buffered peptone water, stomached for1 min in a Model 400 Lab Stomacher (Seward, London,UK), and subsequently incubated for 6 h at 37 �C. Onemilliliter of stomached solution or purge, or 1 g of feces,was placed into an 8-ml tube containing lauryl sul-fate tryptose (LST) broth with 4-methylumbelliferyl-b-D-glucuronide (MUG; REMEL, Lenexa, KS), andincubated at 37 �C for 24 h.After incubation, samples were streaked for isolation

on MacConkey agar (MAC; REMEL, Lenexa, KS) andMacConkey agar with sorbitol (SMAC; REMEL,Lenexa, KS), and incubated for 24 h at 37 �C. Colonymorphology was examined, and typical round, light-colored, smooth colonies were picked from SMACplates and tested for indole production with Kovacsreagent (REMEL, Lenexa, KS). Indole positive colonieswere selected from SMAC plates and transferred totubes with LST broth containing MUG and a Durhamtube. Tubes were observed for gas production andphosphorescence after 24 h of incubation at 37 �C. Gaspositive-phosphorescence negative isolates were agglu-tinated with O157 antisera (REMEL, Lenexa, KS), andO157-positive isolates were streaked on blood agar(REMEL, Lenexa, KS) and incubated at 37 �C for 24 h.One colony was picked from the blood plate and testedfor agglutination with H7 antisera (REMEL, Lenexa,KS). The relative specificity of the serotyping procedureswas greater than 99%.

2.5. Salmonella typhimurium isolation

Procedures for the isolation of S. typhimurium fol-lowed those outlined by Andrews and Hammack (1998).Briefly, 25 g of meat were stomached with 225 ml ofbuffered peptone water as described previously. Onemilliliter of solution (from stomached/incubated meatsamples) or purge, or 1 g of feces, was placed into a 10-mltube of tetrathionate broth (REMEL, Lenexa, KS) forSalmonella enrichment and incubated at 42 �C for 24 h.After incubation, samples were streaked for isolation onbrilliant green agar with novobiocin and XLT-4 agar(REMEL, Lenexa, KS). Colony morphology was com-pared, and three typical round, black (‘‘bull’s-eye’’) col-onies were selected from XLT-4 plates and stab-streakedinto Kigler’s iron agar (KIA) slants (Edge Biologi-cals, Memphis, TN). Then, H2S-positive isolates fromKIA slants were selected and re-streaked on MACand agglutinated with Salmonella O polyvalent (A-E,Vi) antisera (REMEL, Lenexa, KS). Isolates, which

J.R. Davis et al. / Bioresource Technology 84 (2002) 191–196 193

agglutinated with the Salmonella O polyvalent antisera,were further agglutinated with Salmonella group B andD antisera (REMEL, Lenexa, KS). Again, the relativespecificity of S. typhimurium isolation was greater than99%.

3. Results and discussion

In Experiment 1, no S or EC was isolated in the clo-acal swabs of birds or in the floor-drag swabs. Moreimportantly, neither S or EC were isolated from any fecalsamples at any collection period, nor were any S or ECdetected from neck and bung incision samples, purgesamples, and ground beef samples (Table 1). Thesefindings suggest the absence of S and EC in the deep-stacked litter fed to cull beef cows in the experiment. Ourresults concur with those from Georgia, where no S andEC were identified in 86 samples of poultry litter col-lected across the state (Martin et al., 1998), and Cali-fornia, where no S, EC, or Campylobacter was identifiedin 104 samples of stacked-poultry litter from dairy farmsin the San Joaquin Valley (Jeffrey et al., 1998).Within 12 d of deep-stacking the litter, the tempera-

ture of the stack reached 51 �C, and remained elevated(51–59 �C) for the duration of the 21-d stacking process;thus, producing an inhospitable environment for S andEC survival. McCaskey and Harris (1982) found that,when litter inoculated with pathogenic bacteria wasdeep-stacked, heat generated within the stack was suf-ficient to kill all bacteria within 5 d. Kelley et al. (1994)also showed that deep-stacking poultry litter reducedSalmonella spp., Listeria monocytogenes, Staphylococusaureus, and Clostridium perfringens well below their re-spective detection limits, and E.coli was non-culturablein the stacked litter. They too implicated the rise in in-ternal temperature of the stacked litter (Kelley et al.,

1994), as well as possible bacteriostatic properties ofwood shavings (Kelley et al., 1995), as mechanisms forthe decrease in microbial concentrations recovered.Moreover, McCaskey and Gurung (1998) reported thatthe alkaline pH (due to increasing ammonia concen-trations) of properly deep-stacked litter decreases thelikelihood of survival of pathogenic bacteria.In Experiment 2, neither S nor EC were isolated from

fresh litter samples, fecal grab-samples, neck/bung inci-sion samples, purge samples, or ground beef samples(Table 2). Although fresh litter has been shown to har-bor several pathogenic bacteria (McCaskey and An-thony, 1979; Kelley et al., 1994), fecal coliform andstreptococci numbers have been shown to decline rap-idly after surface application of fresh broiler litter ontopastures (Crane et al., 1980). Brown et al. (1980) re-ported that environmental factors, such as temperature,humidity, exposure to sunlight and rainfall, influencethe die-off rate of bacteria on foliage. The increasingambient temperature, as well as increasing day length, oramount of radiant energy of the sun, occurring duringExperiment 2 may have contributed to the failure toisolate S or EC from any sample. Additionally, foragegrowth, albeit quite rapid at the time of Experiment 2,was clipped short by the grazing cows, and Taylor andBurrows (1971) found that cutting forage from pasturesfertilized with municipal sewage greatly reduced thesurvival of E. coli and S. dublin, by altering temperature,increasing evaporative loss (decreasing water activity),and exposing the bacteria to sunlight.Some research has indicated that the bedding mate-

rial (in this case pinewood sawdust) mixed into broilerlitter may have antimicrobial activities. Kelley et al.(1995) reported lower pathogenic bacteria numbers forlitter mixed with wood shavings. Also, lime-treated orconditioned sawdust was shown to reduce Gram-nega-tive and coliform counts when used as bedding in dairy

Table 1

Frequency of isolation of Escherchia coli O157:H7 (EC) and Salmonella (S) from feces, carcasses and ground beef of cows fed either hay or deep-

stacked broiler litter (Experiment 1)

Sample # Positive/# cultured

Hay-fed Litter-fed

EC S EC S

Feces 0/176 0/176 0/176 0/176

Cold water-rinsed

Neck 0/16 0/16 0/16 0/16

Bung 0/16 0/16 0/16 0/16

Trim purge 0/16 0/16 0/16 0/16

Ground beef 0/16 0/16 0/16 0/16

Lactic acid-rinsed

Neck 0/16 0/16 0/16 0/16

Bung 0/16 0/16 0/16 0/16

Trim purge 0/16 0/16 0/16 0/16

Ground beef 0/16 0/16 0/16 0/16

194 J.R. Davis et al. / Bioresource Technology 84 (2002) 191–196

stalls (Hogan et al., 1999). Moreover, it is not uncom-mon for broiler producers to treat broiler-house floorswith antimicrobial and (or) antifungal agents betweenloads of birds. Since the producers where the fresh litteroriginated for this study failed to divulge this informa-tion, we cannot dismiss this type of treatment as aplausible explanation for our negative results.

4. Conclusions

Fresh broiler excreta and fresh broiler litter mayharbor several species of pathogenic bacteria; however,when properly handled, the combination of temperature,alkaline pH, and ammonia concentration that exists inthe stack, as well as the possible bacteriostatic qualitiesof certain bedding materials, contributes to the devel-opment of an environment not optimal for the survivaland reproduction of pathogenic bacteria. Furthermore,while the practice of feeding deep-stacked broiler litter tobeef cattle may not be aesthetically pleasing to somepeople, no research information is available suggesting adirect relationship between food-borne outbreaks fromconsuming beef products and the inclusion of broilerlitter in cattle diets. Results from these experimentssupport the contention that beef cattle, especially thosedestined for ground beef production, may be fed deep-stacked broiler litter or graze pastures fertilized withfresh litter without substantially increasing the likelihoodof carcass, or meat, contamination with S and (or) EC.

Acknowledgements

The authors wish to express their sincere appreciationto the Arkansas Beef Council for financial supportof this project. Additionally, the authors are indebtedto Pete Hornsby, Suzanne Krumpelman, Lillie Rakes,

Matt Stivarius, Joanne Morris, Doug Galloway, andLevi McBeth for assistance with cattle harvest, micro-bial culture, and data collection, and Dr. Zelpha John-son for statistical consultation.

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