E�ect of steam condensation, hot water or chlorinated hot waterimmersion on bacterial numbers and quality of lamb carcasses

C. James *, J.A. Thornton, L. Ketteringham, S.J. James

MAFF Advanced Fellowship in Food Process Engineering, FRPERC, Churchill Building, University of Bristol, Langford, Bristol BS40 5DU, UK

Received 27 August 1999; accepted 9 November 1999

Abstract

Three di�erent systems for decontaminating lamb carcasses immediately post-mortem were investigated; steam condensation, hot

water immersion and chlorinated hot water immersion. All treatments were applied 50 min post-mortem. All three treatments

signi®cantly reduced aerobic plate counts (APC) on the carcasses in comparison with untreated controls. Overall the chlorinated hot

water treatment reduced counts by 1.6 log10 colony forming unit per centimetre square (cfu cmÿ2). There was no signi®cant di�erence

between the steam and hot water treatments with both treatments reducing counts by approximately 1 log10 cfu cmÿ2. No signi®cant

di�erences (P > 0.05) were found in the subjective evaluation of lean appearance, colour appearance, odour, and overall accept-

ability between treated and untreated carcasses after 48 h of chilling and chilled storage. Ó 2000 Elsevier Science Ltd. All rights

reserved.

Keywords: Decontamination; Steam; Hot water; Chlorine; Lamb

1. Introduction

Microbial contamination occurs during many of theseries of slaughtering processes that are required toconvert a live animal to meat suitable for human con-sumption. The muscle tissue of a healthy animal is es-sentially sterile (Gill, 1979, 1980), and most of the initialcontamination of a lamb carcass takes place during¯eece removal and evisceration. Reducing surface con-tamination would improve food safety and extend shelflife. James and James (1997) have extensively reviewedthe range of surface decontamination methods that mayhave application to red meat.

Steam has been shown to be e�ective in reducing thenumber of microorganisms on meat surfaces (Biemuller,Carpenter & Reynolds, 1973; Karmas, 1975; Morgan,Goldberg, Radewonuk & Scullen, 1996a; Morgan,Radewonuk & Scullen, 1996b; James et al., 1998). Onpork carcasses, reductions in psychrophilic counts ofapproximately 3±4 log10 colony forming units per gram(cfu gÿ1) when compared to untreated samples werereported by Karmas (1975). Smith and Graham (1978)also showed that hot water immersion of mutton car-

casses could reduce Escherichia coli counts by 3 log10

units. In addition, the antibacterial action of chlorinetogether with hot water has been investigated. Kotula,Lusby, Crouse and de Vries (1974) reported that wash-ing beef forequarters with chlorinated water (200 ppm)could reduce total aerobic counts by up to 5 log units.

However, decontamination systems may also ad-versely a�ect qualities that control carcass acceptability,i.e., ÔbloomÕ, colour and odour (Patterson, 1968; Bailey,1972; Bailey & Roberts, 1976). Bloom is a very subjec-tive judgement of the overall attractiveness of the car-cass. High pressure cold water sprays may adverselya�ect bloom and hot water immersion a�ects colour(Bailey, 1972). An e�cient decontamination systemshould reduce bacterial numbers without any detri-mental changes to the appearance of the carcass.

The aim of this study was to compare three potentialmethods of decontaminating lamb carcasses. The threesystems were: atmospheric steam at 100°C, immersion in90°C water and immersion at the same temperature inwater containing 250 ppm free chlorine. All treatmentswere applied for 8 s. Preliminary investigations had in-dicated that exposure time more than this would pro-duce unacceptable surface changes on exposed muscletissue. The e�ect of the di�erent treatments on microbialnumbers, appearance, odour, and overall acceptabilitywere all assessed.

Journal of Food Engineering 43 (2000) 219±225

www.elsevier.com/locate/jfoodeng

* Corresponding author. Tel.: +44-117-928-9239; fax: +44-117-928-

9314.

E-mail address: chris.james@bristol.ac.uk (C. James).

0260-8774/00/$ - see front matter Ó 2000 Elsevier Science Ltd. All rights reserved.

PII: S 0 2 6 0 - 8 7 7 4 ( 9 9 ) 0 0 1 5 5 - 7

Overall, the aim of this work was to produce lambcarcasses that would have the acceptable quality traitswhich retailers and consumers expect of fresh lamb to-gether with signi®cantly decreased microbiologicalcounts.

2. Materials and methods

2.1. Pre-slaughter handling of lambs

Thirty-two spring lambs (carcass weights of 17±24 kg)were delivered in groups of eight to the Universityabattoir. Each group was held in the lairage pens of theabattoir for 24 h before slaughter. Each group of eightwas subjected to one of the three decontaminationtreatments or used as the control.

2.2. Slaughter procedure

The lambs were inspected ante-mortem by an o�cialveterinary surgeon (OVS) for both state of health, wel-fare and age recognition dentition. The lambs were thenelectrically stunned using a 120 V head only stunner andbled. The order in which the lambs were slaughtered wasrandom, the selection being carried out by the abattoirsta�.

Electrical stimulation was carried out 1 min afterslaughter using low voltage (70 V; 16.7 Hz) for 60 s. Twoelectrodes were inserted into the muscle of the hindlimbs near the Achilles tendon, two inserted in themuscle of the forelegs and a clip attached to the nose ofthe lamb. Electrical stimulation was carried out to re-duce the risk of cold shortening of the muscle ®bres inthe lambs during chilling.

2.3. Dressing procedure

Immediately after electrical stimulation the carcasseswere eviscerated and dressed. Following dressing thecarcasses were manually spray washed, using a fan jet ata line pressure of 230 kN mÿ2 with cold �15� 2°C�potable water, for approximately 15 s. All the carcasseswere health marked, classi®ed for conformation andscored for the development of fat cover relative to thedimensions of the carcass.

2.4. Decontamination procedures

Treatments were all carried out in a processing halladjacent to the abattoir. All treatments were carried outfor 8 s. Exposure times (8 s) were controlled manuallyand measured using a stop watch. The loading andunloading operations were performed in <1 s. Aftertreatment the carcasses were allowed to drain for 5 minbefore bacterial samples were taken (55 min post-

mortem). Following sampling, temperature probes wereinserted into the deep leg of the carcasses and they wereplaced in a commercial chiller operating at 1:5� 2:5°C.

2.4.1. Control groupMicrobial samples were taken aseptically at 55 min

post-mortem. The carcasses were then chilled in thesame manner as the treated carcasses.

2.4.2. Atmospheric steam vesselA simple atmospheric steam pilot plant was designed

and constructed for the investigations. Its essential fea-tures are shown in Fig. 1. The processing vessel itselfwas constructed from a 250 l plastic barrel with thebottom cut-o� and extended with a long black plasticcurtain. This produced a cylindrical working sectionapproximately 2� 0:6 m2 diameter. The vessel wassuspended from a surrounding frame by three steelwires. Steam (from a steam line operating at 500 kNmÿ2) entered the top of the vessel through a valve andwas evenly distributed into the working section througha ba�e. The ¯ow of steam into the section was con-trolled by a hand-operated valve. Before each trial,steam was used to ¯ush out any entrained air at thebottom of the vessel and then its ¯ow was adjusted toproduce a non-turbulent ¯ow within the workingsection.

Lambs were raised into the vessel using a manualhoist. The lamb carcass was suspended by the hind legson a gambrel that was attached to a wire running upthrough the steam chamber, through the ba�e and outthrough a small hole in the top of the steam chamberwall. The wire was greased so that it ran easily through

Fig. 1. Schematic of atmospheric steam decontamination system.

220 C. James et al. / Journal of Food Engineering 43 (2000) 219±225

the holes in the ba�e and the top of the chamber. Acounter weight at the other end of the wire enabled thecarcasses to be easily raised or lowered. The 8 s cycletime was measured from the time the carcass was totallyimmersed in the steam to the start of the removaloperation.

2.4.3. Hot water immersionThe pilot plant for the immersion treatments con-

sisted of a cylindrical, insulated metal vessel containingpotable water at 90°C. The tank held approximately 300l of water when full. The hoist system used in the steamtreatments was slightly modi®ed to allow the carcass tobe lowered into the immersion tank. Before each treat-ment the water was heated to 90°C using direct steaminjection. The insulated vessel maintained the watertemperature at 90� 1°C during each treatment.

Due to their natural buoyancy the lamb carcassesneeded to be weighted down to stop them ¯oating in thetank. A 5 kg weight, vacuum packaged to avoid con-tamination, was placed in the body cavity of each car-cass prior to immersion. The 8 s cycle time wasmeasured from the point the carcass was totallyimmersed in the water to the start of the removaloperation.

2.4.4. Immersion and chlorineThe same immersion tank vessel as described in

Section 2.4.3 was used. A previously calculated amountof sodium hypochloride (Deosan sodium hypochloride(NaOCl)) was mixed together with hot water at 90°C toproduce a concentration of 250 ppm free chlorine.

The calculation of the concentration of free chlorinein the immersion tank was checked using chlorine watertesting tablets (PalintestÓ) and adjusted if required byadding more sodium hypochloride. The tablets werecrushed and stirred into a sample of the chlorinatedwater until a colour change occurred. The number oftablets required to create this colour change was used tocalculate the chlorine content in parts per million ormilligram per litre.

Immediately before each trial, the concentration wasin the range 250� 10 ppm free chlorine. As before, the 8s cycle time was timed from the point at which thecarcass was totally immersed in the water to the start ofthe removal operation.

2.5. Microbiological sampling and analysis

All carcasses were sampled on two sites 5 min aftertreatment (55 min post-mortem):1. The abdomen, approximately 2 cm above the ventral

midline. This was chosen as it was the point where in-cision occurred during the removal of the breast stripof the ¯eece.

2. The neck region, 1 cm above the atlas axis neck/headjoint. This was chosen since it was the point where thehand of the slaughterman directly contacted the necksurface tissue during the process of removing thehead from the carcass.

Sampling was undertaken using the wet and dry swab-bing method described by Kitchell, Ingram & Hudson(1973). A 10 cm2 area delineated by a sterile metaltemplate was used. A swab (Medical Wire, MW 104)was moistened in diluent (90.1% peptone, 0.85% NaCl),and the sampling site swabbed in a standard mannerusing 10 horizontal and 10 vertical passes over a previ-ously de®ned area inside a l0 cm2 template. The swabwas broken o� into diluent (90.1% peptone, 0.85%NaCl). The swabbing was then repeated using an un-moistened swab, which was broken o� into the samediluent as the ®rst. The diluent used was 10 ml peptidesaline contained in a universal bottle (McCartney) with4±5 glass beads. These were stored in a commercial chillroom operating at 1:5� 2:5°C for a maximum of 2 hbefore microbiological examination. To reduce the errorintroduced by manual sampling techniques, all swabsamples were taken by the same individual.

Appropriate serial dilutions were done and plated onTryptone Soy Agar (TSY Lab M) to determine theaerobic plate count (APC). The plates were incubatedfor 48 h at 30°C. TSY agar was used in preference toplate count agar (PCA) since it is more suitable for re-covering heat damaged cells (Corry, 1999). Counts werecalculated as colony forming units per centimetre square(cfu cmÿ2) using the surface counting method.

2.6. Carcass quality assessment

All carcasses were assessed after 48 h in chilling/storage by a ®ve member panel, who were selected fortheir ability to detect visual variations betweencarcasses.

The carcasses were randomly presented in groups offour (all treatments were included) under the same il-lumination (northern daylight lux). The assessmentswere made simultaneously by all members, but withoutany discussion among them. The carcasses were assessed

Table 1

Six-point scales used to access carcass quality after 48 h

Six-point scale

1 6

Lean appearance Very dehydratzed Very fresh

Colour appearance Very dark Milky white

Odour assessment Very stale Very fresh

Overall acceptability Dislike intensely Like intensely

C. James et al. / Journal of Food Engineering 43 (2000) 219±225 221

for lean appearance, colour, odour and overall accept-ability using a 6-point hedonic scale (Table 1).

2.7. Statistical analysis

All results were analysed using a one-way analysis ofvariance (ANOVA) and two-way (ANOVA) analysis ofvariance contained in a MinitabÓ software package.

3. Results

3.1. Total viable counts at 55 min post-mortem

The mean APC at the two sampling sites for thecontrol and three decontamination treatments areshown in Table 2. Mean counts from the control samplewere 2.93 and 3.51 log10 cfu cmÿ2 on the neck and ab-domen, respectively.

In all cases, the mean APC on the abdomen washigher than that from the neck sample. The di�erencesvaried between 0.04 and 0.58 log10 cfu cmÿ2 with anoverall mean di�erence of 0.19 log10 cfu cmÿ2.

Statistical analysis of the results showed that for eachsampling site the mean counts were signi®cantly lower�P 6 0:05� for the treated carcasses than the controls.Overall, the combination of hot water with chlorineresulted in a statistically lower �P 6 0:05� count than thehot water or steam treatments.

The largest reduction of 1.86 log10 cfu cmÿ2 wasachieved on the abdomen when the carcass was treatedwith the hot water and chlorine combination (Table 3).The lowest reduction of 0.79 log10 cfu cmÿ2 was mea-sured on the neck of steam-treated samples. Overallcounts on carcasses treated with hot chlorinated waterwere 1.6 log10 cfu cmÿ2 lower than on controls. Overallcounts on steam and hot water-treated carcasses were

slightly higher, being about 1 log10 cfu cmÿ2 lower thancontrols.

3.2. Chilling rate

The temperature in the deep leg of the lambs wasreduced to 7°C by approximately 5.2 h post-mortem.

3.3. Carcass quality

There were no signi®cant di�erences (P > 0:05) in theobjective evaluation of lean appearance, colour, odour,and overall acceptability between treated and controllamb carcasses after 48 h chilling and storage (Table 4).

3.3.1. Control carcassesThe control carcasses appeared ÔnormalÕ with the vi-

sual quality traits of young lamb after chilling. Theattractive bright, cherry red colour associated withfreshness was visible in all carcasses.

3.3.2. Atmospheric steam-treated carcassesSteam-treated carcasses were considered acceptable.

Greying or bleaching of the carcass surface was notice-

Table 2

Mean APCs at two sampling sites on lamb carcasses subjected to three di�erent decontamination treatments A

Treatment APC, log10 cfu cmÿ2; S.D., n� 8

Sample site Overall

Neck Abdomen

Hot water (90°C) containing chlorine (250 ppm) 1.57a (0.13) 1.65a (0.36) 1.61a (0.24)

Steam 2.14b (0.21) 2.18b (0.26) 2.16b (0.23)

Hot water (90°C) 2.l0b (0.43) 2.16b (0.22) 2.13b (0.32)

Control 2.93c (0.21) 3.51c (0.33) 3.22c (0.27)

Standard error of di�erence of means (s.e.d.) 0.13 0.15

Least signi®cant of di�erence (l.s.d) 0.26 0.30

Overall site mean 2.18 (0.24) 2.37 (0.29)

Overall site median 2.16 2.38

A Means with di�erent superscripts in same column are signi®cantly di�erent (P < 0:05).

Table 3

Reduction in APCs, in comparison with no treatment, on lamb car-

casses subjected to three di�erent decontamination treatments

Treatment APC, log10 cfu cmÿ2; n� 8

Sample site Overall

Neck Abdomen

Hot water containing

chlorine

1.36 1.86 1.61

Steam 0.79 1.33 1.06

Hot water 0.83 1.35 1.09

222 C. James et al. / Journal of Food Engineering 43 (2000) 219±225

able immediately after steam treatment. However,acceptable colour returned after chilling and storage for48 h.

3.3.3. Immersion-treated carcassesImmersion-treated carcasses were considered accept-

able. Immediately after treatment, while the carcasseswere draining, they had a slightly cooked appearance onthe thin edges and exposed cut muscle surfaces. This wasespecially noticeable on the exterior panniculua ÔbarkÕmuscle surface and the interior (thorax, kidneys andabdomen) of the lamb carcasses. In general, acceptablecolour returned after chilling and storage for 48 h.

3.3.4. Immersion and chlorine-treated carcassesImmersion/chlorine-treated carcasses were considered

acceptable. Immediately after immersion in the hotchlorine solution, the lamb carcasses appeared slightlypaler than the control carcasses. Furthermore, exposedcut surfaces such as the sternum (brisket) seemed tohave a slightly cooked appearance, as did the pan-niculua muscle on the external surface of the carcass.The interior of the carcass (thorax, kidneys and ab-domen) also had a slightly cooked appearance. This wasespecially visible on the kidneys. These changes were notnoticeable after chilling and storage for 48 h.

4. Discussion

There is general agreement that the main source ofbacterial contamination on a meat carcass is from theanimals themselves. At the point of slaughter the mus-culature of the animal is e�ectively sterile and initialcontamination occurs on the exposed surface. The mainsources of contamination are the skin, hooves, etc., ofthe animal; faeces voided by the animals; bacteria de-rived from the opened gut; and soil, dust, etc., carried tothe killing-¯oor. Two main routes of contaminationhave been identi®ed:1. Deposition of bacteria scattered in the air and splash-

ing with contaminated faeces, etc.2. Contact with dirty instruments, hands, clothes, etc.In the UK the meat industry has invested considerabletime and e�ort into methods of reducing bacterial cont-amination on the live animal and throughout the

slaughter process. It is therefore very disappointing thatthe last published scienti®c survey (Hinton, Hudson &Mead, 1998) reported that ÔIt can, therefore, be safelyconcluded that there is little evidence of any majorchange in the bacteriological quality of British beefduring the last 10±15 yearsÕ.

The limited success in reducing contamination hasfocussed attention on means of decontaminating meat.The government authorities in the USA were the ®rst toencourage the routine use of decontamination systems inmeat plants. As a result of this work many US meatcompanies are commissioning decontamination systemsand obtaining approval for their use. The most suc-cessful commercial systems appear to be large automaticpressurised steam systems with processing times of 8±10 s(Nutsch et al., 1997; Phebus et al., 1997; Nutsch et al.,1998). Reductions of about 3.5 log10 cfu cmÿ2 (for spe-ci®c organisms on inoculated beef carcasses) and1 log10 cfu cmÿ2 (for naturally occurring bacterial pop-ulations on beef carcasses) have been claimed for thesesystems. However, no published data have been foundfor their use with lamb carcasses.

In the present investigations the work was carried outon whole lamb carcasses slaughtered and processed innear commercial conditions. The most comparablepublished work is that by Bailey (1971, 1972) and Kelly,Dempster and McLoughlin (1981) and Kelly, Lynch andMcLoughlin (1982) relating to spray washing, Smithand Graham (1978) on immersion, and Dorsa, Cutter,Siragusa and Koohmarie (1996) on steam. In BaileyÕsstudies reductions of between 0.6 and 0.8 log10 per car-cass were achieved. Kelly et al. (1981) found that watertemperatures of P80°C were required to obtain reduc-tions of P1 log10 cfu cmÿ2, from initial counts of be-tween 3.2 to 4.2 log10 cfu cmÿ2. Trials by Smith andGraham (1978) on naturally contaminated carcassesreduced counts from around 3.9 to 2.5 log10 cfu cmÿ2 byimmersing in water at 80°C for 10 s. In the work ofDorsa et al. (1996) work reductions of up to 1.7 log10 cfucmÿ2 were achieved using steam for 30 s and ®nal APCsranged from 1.2 to 0.9 log10 cfu cmÿ2. The resultsachieved in these experiments are therefore very similar.

Although all treatments had an immediate a�ect onthe appearance of the carcasses, such changes were notpermanent and treated carcasses recovered an accept-able appearance within 48 h. Similar observations have

Table 4

Mean overall appearance scores (S.D.) for treated and untreated lamb carcasses at 48 h post-mortem

Control Steam Hot water Hot water/chlorine

Lean 4.33 (0.92) 3.75 (1.03) 4.13 (0.94) 4.25 (0.81)

Colour 3.33 (0.80) 3.45 (0.81) 3.60 (0.96) 3.73 (0.91)

Odour 4.43 (0.98) 4.73 (0.88) 4.53 (1.01) 4.75 (0.74)

Acceptability 4.60 (0.87) 4.45 (0.90) 4.73 (0.82) 4.73 (0.82)

C. James et al. / Journal of Food Engineering 43 (2000) 219±225 223

been noted by other studies (Bailey, 1971, 1972; Smith &Graham, 1978; Dorsa et al., 1996).

Immersion in water at 90°C containing 250 ppm freechlorine produced the highest reductions and lowest ®-nal counts. However, it is unlikely that the use ofchlorine in concentrations above 200 ppm would bepermitted on meat within the European Union unless itproduced a signi®cant advantage in terms of food safety.Even if chlorine was allowed then there are manypractical problems that would have to be overcome,including the control of chlorine levels, the protection ofdelivery systems from corrosion, and protecting thesafety of workers.

Immersion in water at 90°C and treatment with con-densing steam at 100°C produced very similar reduc-tions. Neither system was optimised, agitating the waterin one, and improving the steam distribution in the sec-ond, would probably improve their performance. Incommercial application, the immersion system presentsproblems in terms of ®ltering, recirculating the water and®nal disposal of the water. The buoyancy of meat car-casses also poses a particular practical problem. Inher-ently the use of atmospheric steam is the more attractiveoption for commercial use, due to its simplicity.

5. Conclusions

This work demonstrated that decontaminationtreatments are, and can be, e�ective in reducing totalviable microbial counts on lamb carcasses without sig-ni®cantly a�ecting carcass quality. Immersion in waterat 90°C containing 250 ppm free chlorine reduced APCsby 1.6 log10 cfu cmÿ2. The steam and hot water treat-ments were slightly less e�ective but still reduced mi-crobial counts by approximately 1 log10 cfu cmÿ2. In allcases the counts on the treated carcasses were substan-tially lower than those produced by most conventionalabattoirs. In all cases there was no signi®cant di�erencebetween treated and untreated carcasses in terms of leanappearance, colour appearance, odour, and overall ac-ceptability after 48 h of chilling and chilled storage.

It is likely that legislation and consumer concern willlimit the use of chemicals such as chlorine in decon-tamination applications. Producing and maintainingwater at 90°C is far less energy intensive than producingsteam at 100°C. However, less steam is required toachieve the same e�ect and there are more problems in®ltering the water, cleaning and water disposal in theimmersion system. We would therefore conclude thatthe steam system shows the greatest potential in an in-dustrial application.

The position of the sampling site directly a�ects themeasured reduction in APCs. In both the immersiontreatments, the abdomen had a longer processing timethan the neck due to the method of hoisting the carcass

from the hindlegs. The opposite was the case for thesteam treatment. Further development is required toovercome this problem and optimise the steam distri-bution and design of a commercial system.

Acknowledgements

The authors would like to thank the management andsta� of the University abattoir. Especially Mr. A. Fisher,for carrying out the lamb carcass classi®cation. Dr. I.Richardson, for providing advice on electrical stimula-tion. Messieurs N. Ebdon, M. Osborne and D. Brock,for work in processing the lambs. We would also like tothank and express our appreciation to Dr. J. Corry andMr. W. R. Hudson, for their advice with the microbialanalysis.

Finally, we would like to thank Anglo Beef Proces-sors Ltd, especially Mr R.M. Cracknell, Chief Execu-tive, and Mr. D. Lindars, Group Technical Manager,for their ®nancial assistance towards this project.

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