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Research into poultry meat qualityM.A. Grashorn aa Department of Poultry Science , University of Hohenheim , Garbenstrasse 17, 70599Stuttgart, GermanyPublished online: 12 Aug 2010.

To cite this article: M.A. Grashorn (2010) Research into poultry meat quality, British Poultry Science, 51:S1, 60-67, DOI:10.1080/00071668.2010.506761

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British Poultry Science Volume 51, Supplement 1 (August 2010), pp. 60—67

Research into poultry meat quality

M.A. GRASHORN

Department of Poultry Science, University of Hohenheim, Garbenstrasse 17, 70599 Stuttgart, Germany

Abstract 1. Research in the field of poultry meat quality has become more varied during the last 50years. Besides meat content and microbial condition, animal welfare issues during the slaughter process,muscle morphology, physiology of meat ripening, impact of slaughter process on meat quality, sensoryattributes of meat and meat processing have come into focus.2. The present review summarizes findings and developments in the fields of muscle physiology, meatripening and meat quality aberrations (like PSE), nutrient composition and sensory qualities, effect ofthe slaughter process on carcass and meat quality, hygienic conditions and product safety duringslaughtering, all based on selected papers published in British Poultry Science during the last 50 years.3. Some special findings and conclusions are lifted out of the whole results presented in the papers toindicate their importance and to show their contribution to the development of knowledge in therespective field.

Intensive research on poultry meat qualitystarted after World War II, mainly in industria-lised countries. At that time the main objectiveswere to satisfy the increasing demand for animalprotein in human nutrition and to increase thesafety of meat. Thereafter, research in the fieldbecame more wide-ranging. In addition to meatcontent and microbial condition, animal welfareissues during the slaughter process, musclemorphology, physiology of meat ripening,impact of the slaughter process on meat quality,sensory attributes of meat and meat processingall became important. The increase in theincidence of carcase and meat quality aberrationsrelated to increased broiler growth rate andincreased numbers of birds fattened and slaugh-tered is particularly marked. This change inresearch is also reflected in the topics of paperspublished on poultry meat quality in BritishPoultry Science (BPS) during its 50-year history.

More than 200 papers have been publishedin BPS on this topic to date, making it impossibleto consider all of them in a review. I thereforegive a compact overview of these developments,based on selected papers published in British

Poultry Science and highlight exemplary advances.Out of the huge number of topics, four havebeen chosen which are of major importance:(i) muscle physiology, meat ripening and meatquality aberrations such as PSE (pale, soft,exudative) meat, (ii) nutrient composition andsensory attributes, (iii) effect of the slaughterprocess on carcase and meat quality, and (iv)hygienic conditions and product safety duringslaughtering. Effects of management factors suchas genetics, husbandry conditions, feeding, willbe considered where appropriate. A short sum-mary of the current state of knowledge isprovided for all points and special advances inunderstanding and knowledge are highlighted bypapers published in BPS, including verbatimcitation of key passages.

MUSCLE PHYSIOLOGY AND MEATRIPENING

Muscle composition and muscle physiology areimportant starting points for the development ofedible meat. Many experiments have been

Correspondence to: M.A. Grashorn, Department of Poultry Science, University of Hohenheim, Garbenstrasse 17, 70599 Stuttgart, Germany.

E-mail: michael.grashorn@uni-hohenheim.de

ISSN 0007–1668(print)/ISSN 1466–1799 (online)/10/0S10060—8 � 2010 British Poultry Science LtdDOI: 10.1080/00071668.2010.506761

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conducted in the past to investigate the impor-tance of the ante mortem muscle metabolism onpost mortem biochemical processes and identifythe factors which affect these processes.

In general, meat is the edible form of themuscle tissue of animals. The muscle tissueconsists of muscle fibres, connective tissue andfat. The number of muscle fibres is already fixedat hatching and the increase in the muscle mass iscaused by enlargement of the diameter of musclefibres. Muscle fibres are bundles of muscle cellswhich are surrounded by the endomysium. Inpoultry, thigh muscles and back musclescontain more connective tissue and fat thanbreast muscles. Breast muscle consists only ofwhite muscle fibres (fast twitch, �B), whereasthigh muscle contains both red (fast-twitch, �R)and white fibres (�B).

After the birds are slaughtered muscles areconverted to edible meat by the process of meatripening. During meat ripening energy resources(glycogen, ATP, CK) of muscles are degradedand the resultant biochemical processes provokesignificant changes in the structure of musclesresulting mainly in the denaturation of muscularproteins. The different steps of meat ripening areexemplified by the stiffening of the muscles afterdeath, in combination with muscle shortening.This is followed by a phase of softening again.The process of stiffening is defined as ‘‘rigormortis’’ and is normally reached in most animalspecies after some hours. Both ante mortem andearly post mortem conditions may influence theripening process significantly.

Shrimpton (1960) described the process ofmeat ripening in the very first issue of BPS andfound that both the fasting of birds beforecatching and scalding conditions during slaugh-tering were factors affecting the ‘‘chemicalchanges associated with rigor mortis and thetenderness of the flesh’’. Shrimpton found that‘‘under commercial conditions rigor can beexpected to develop within 10 minutes of slaugh-ter unless the birds have been specially starved’’.He concluded further that the assumption ‘‘thatthe rate of post mortem glycolysis in muscle isnecessarily the same in poultry and mammals, isshown to be false’’. These basic findings are stillvalid today, whereas his observation that‘‘none of the factors known to be associatedwith the onset of rigor can therefore by expectedto have any substantial effect on the tendernessof the meat from young chickens’’ cannot becompletely accepted. It is unquestionable that‘‘adverse conditions during the life of the bird’’(Shrimpton, 1960) may negatively affect tender-ness of the meat and ‘‘may also be accentuated bybad practice in the packing station’’. Shrimptondid not attribute the term ‘‘stress’’ to thementioned ‘‘adverse conditions’’ in his paper

and he was not able to explain in more detail therelationship between the course of meat ripeningand the texture of the edible meat. It took severalyears to add significant new knowledge to thisfield.

Duncan et al. (1986) showed that catchingconditions (manually versus machine) signifi-cantly influenced ante mortem metabolic condi-tions and in this way impaired meat ripening.These authors reported that manual catching hadsevere stress effects, because the degradation ofenergy resources was accelerated, resulting inchanged biochemical processes during meatripening. An important point is that themethod of handling birds during catching is notonly relevant for meat quality but also representsan animal welfare issue. Catching birds by oneleg, transporting them head upside down incrowded groups and throwing them rapidly intotransport boxes is a very frightening situation forbirds which may also cause pain and even injuriesto them. In the same way, handling of birdsbetween arrival in the slaughter house and killingmay impose severe stress, pain and anxiety. Formany years electrical water bath stunners havebeen used in poultry slaughter houses: birds areshackled alive after unloading from transportboxes and are moved in a belt head down forseveral seconds to stunner and killer.

The stress conditions due to handling incombination with the stunning conditions are themost challenging factors during slaughtering (Rajet al., 1990, Raj and Johnson, 1997), significantlyaffecting degradation of glycogen resources inmuscle tissues and thereby the process of meatripening. Normally, accelerated post mortem gly-colysis is expected to result in tougher meat, asdescribed for stress-related acceleration of bio-chemical processes after death of birds. Raj et al.(1990) found that after argon stunning broilermeat was more tender in comparison to electricalstunning, despite accelerated glycolysis. Theyassumed that ‘‘it is possible that in argonstunning anaerobic glycolysis may start beforethe broiler has died, and that the anoxicconvulsions occurring during stunning will accel-erate the onset of rigor mortis’’ and stated that ‘‘apossible explanation for this is that wing flappingin broilers is an act very similar to that of flightand the breast muscles are morphologicallydesigned to cope with it, irrespective of itsseverity over a short duration. On the contrary,the tonic muscular spasm induced by electricalstunning appears to be relatively more detri-mental to meat quality’’. In summary, stressduring ante mortem handling of birds and induc-tion of muscular spasm during stunning in theslaughter process both significantly influence theprocess of meat ripening and may lead to meatquality defects such as pale, soft, exudative (PSE)

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condition in chicken and turkey breast meat. PSEmeat is difficult to process satisfactorily and maybe unsuitable for human consumption so thecondition is thus of economic relevance.

The reasons for PSE are still not clear but upto 30% of broiler breast meat and up to 40% ofturkey breast meat can show this aberration incommercial slaughter houses (Barbut, 1997a,b;Zhang and Barbut, 2005). In pork meat produc-tion PSE was a big problem during in the 1980sand 1990s. In pigs, PSE meat can be easilyidentified by measuring pH, conductivity and/orbrightness 45 min post mortem in back muscle. Incontrast to pork, pH and conductivity are lessreliable indicators of PSE in poultry breastmuscles, although Zhang and Barbut stated in2005 that ‘‘both L* and pH values can be used asa predictive tool in sorting chicken breast fillets’’.In several studies in commercial poultry proces-sing plants Barbut used only brightness (L*-valueaccording to CIE) as indicator of PSE in chickenand turkey meat and found high correlationsbetween L*-value (15. min pm.) and waterholding capacity (WHC) and/or texture. Incommercial poultry processing plants meat qual-ity status is important for further processing andthus plants should have a simple tool todetermine this status as early as possible in theslaughter process. If the status is known early‘‘PSE meat can thus be either blended with othermeats to mask its deficiency, or diverted to lowinjection rate products’’ (Barbut, 1997a). For thispurpose a truncation (cut-off) point has to bedefined for the L*-value. Barbut suggested ‘‘thatthe exact L* value of the cut-off point should bedetermined by each plant depending on itsparticular processing requirements’’. Suitabletruncation points could be �49 for broilers(Barbut, 1997a) and �48 for mature turkeyhens (Barbut, 1997b).

With further processing certain meat treat-ment after harvesting may intensify the negativefeatures of PSE meat. Zhang and Barbut (2005)reported that freezing further reduces the func-tionality of PSE chicken breast meat. Comparableeffects were found with chilling in turkeys:Wynveen et al. (1999) observed a rapid declineof pH in breast muscle within the first 9 minpost mortem. This led to extensive protein dena-turation and they stated that ‘‘such proteindenaturation can lead to the loss of functionalitywhich is considered to be the primary factorassociated with the development of PSE char-acteristics’’. The application of ‘‘snow chilling’’with CO2 intensified meat quality abnormalities.Thus, Wynveen et al. (1999) concluded that ‘‘theuse of CO2 snow to chill breast meat for shippingcontributed to PSE-like characteristics by decreas-ing water holding capacity’’ and that ‘‘furtherinvestigation is needed’’ to analyse these effects

in more detail. In general, it is a well knownphenomenon in poultry meat processing thatearly and intensive chilling may result in coldshortening of the muscles. Cold shortening aswell as rigor shortening retards rigor mortis whichresults in impaired meat texture. The poultryslaughtering process is characterised by a shortprocessing time and carcases may enter thechiller before the onset of rigor. These relation-ships have been analysed in detail by Dunn et al.(1995), who concluded that ‘‘the evidence sug-gests that both rigor and cold shortening exert animportant influence on the textural variability ofPM (pectoralis major) muscles from whole broilercarcases chilled under normal conditions. Therisk of rigor shortening may be lowered bycooling rapidly in water at 4�C. However, fastair chilling at �12�C might be more acceptablecommercially and also appears to minimise therisk of rigor shortening. Nevertheless, rapid air-chilling at �12�C does not lower overall texturalvariability and toughness because it alsoenhances the risk of adverse cold shortening incarcases with pH15 values �6�7’’.

The development of rigor mortis depends onthe rate that glycogen resources are degradedand the metabolic activity of muscle tissue.Because pH decline and meat quality differ inpoultry species with different growth rates it hasto be assumed that a general relation existsbetween growth rate and meat ripening.Fernandez et al. (2001, 2002) observed cleardifferences in the glycogen content of differentturkey muscles between slow and fast growingturkey breeds but no differences in ultimate pHwere detected (Fernandez et al., 2001). Theyconcluded that ‘‘any variation in glycogen con-tent above the threshold corresponding to thecessation of glycolysis may not be related todifferences in ultimate pH’’ and that ‘‘our studydoes not support the idea that genetic selectionon growth performance enhances the rate of postmortem changes in turkey breast muscle’’. Thiswas confirmed by the lack of significant differ-ences in meat quality features, such as drip lossand texture, in the three tested lines. Theyconcluded that ‘‘the water holding capacity offresh and cured-cooked meat was not related tothe rate and extent of post mortem pH fall,suggesting that other muscle characteristicswould determine the quality of turkey breastmeat’’ (Fernandez et al., 2001). In another studyFernandez et al. (2002) observed a distinctrelationship between live weight of turkeys andthe rate of post mortem pH fall, which had notbeen previously reported in poultry. They statedthat ‘‘our results confirm that, under commercialprocessing conditions, the technological yield ofcured-cooked turkey meat is negatively related tothe rate of post mortem pH fall, as is the case in

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pork’’. Furthermore, they estimated that a 1-unitdifference in pH20 corresponds to a two-pointdifference in the technological yield. This under-lines the necessity in poultry processing to selectthe raw meat on the basis of the rate of postmortem pH fall (Fernandez et al., 2002).

NUTRIENT COMPOSITION AND SENSORYATTRIBUTES OF MEAT

Nutrient composition is an important meatquality feature with regards to human nutrition.In general, meat is composed of water, protein,fat and collagen. In the past, many attempts havebeen undertaken to increase leanness in poultry.Feeding was the first target of studies.Optimising the nutrient composition of diets,introduction of adapted feeding programmes(phase feeding) and application of feed restric-tion (qualitative and quantitative restriction, skip-a-day) have been identified as useful tools incontrolling fatness of carcases. However, thetendency for birds to deposit fat is geneticallydriven, indicating that fatness and/or leannesshave to be modified at the breeding level forsustainable improvement.

Several selection experiments have beenconducted to directly reduce fatness in broilersusing special tools for measuring abdominal fatin vivo (fat calliper) and/or to estimate meatcontent or meat yield in vivo (ultrasound). In thelate 1970s Griffin and Whitehead initiated aselection experiment in broilers using plasmavery- low-density-lipoprotein (VLDL) concentra-tion as a selection criterion for leanness inbroilers (Whitehead and Griffin, 1984). Due tothe high estimated heritability of plasma VLDLconcentration (mean h2

¼ 0�50) a distinct separa-tion of low and high fat line was achieved both forthe selection criterion and for leanness. As the fatcontent diminished in the lean line, protein andash content increased. Therefore, they concludedthat ‘‘plasma VLDL selection method presentlyemployed is sufficiently simple to be applied on acommercial scale and provides an alternative tothe expensive nutritional methods of controllingexcessive fat deposition in broilers. The leanerbroilers resulting from selective breeding havethe added economic benefit of superiorFCE . . . but organoleptic factors may ultimatelybecome limiting from the commercial point ofview’’. Here the authors foresaw that a veryextreme reduction in fatness will negativelyaffect sensory attributes of the meat due to thetaste relevance of lipid components.

Sensory attributes are the most importantfeatures of meat for consumers. Appearance(including shape and colour), odour and taste(including juiciness and tenderness) are the main

descriptors of poultry meat sensory features.Changes in sensory attributes have to beexpected with breeding for either leanness orincreased muscle mass. Fernandez et al. (2001)reported differences in the collagen content ofmuscles in turkeys with different growth rates.Slow-growing birds showed a higher collagencontent than fast growing ones. The authorsconcluded that ‘‘the higher collagen content inthe SG (slow growing) line may be attributed tothe lower cross sectional area (CSA) of musclefibres, leading to a higher content of endomysialcollagen relative to muscle volume’’. Accordingto Roy et al. (2006) age-related changes incollagen content are very small in chickenscompared to mammalian species, but supplyinghigh dietary energy enhances the deposition ofinsoluble collagen. In the study of Roy et al.‘‘chickens fed on high energy diets had thickperimysia with large collagen fibres composed ofcompact accumulated fibrils’’. They summarisedtheir findings as ‘‘although the total amount ofcollagen did not differ among the chickengroups, their intramuscular architecture diddiffer. The rapid growth rate of the pectoralismuscle induced by feeding high nutritional valuediets was accompanied by myofibre hypertrophyand the development of large perimysial collagenbundles or fibres’’. In conclusion, an increase incollagen results in tougher meat.

For a long time it was believed that theamino acid content and composition in tissuewas hardly altered by feeding of birds due to theRNA-dependent process of protein formation,while the total protein content of muscle tissueswas directly reflected by muscle mass. Now,recent research on branched-chain amino acids(BCAA such as leucine, isoleucine, valine), inview of their role in the sensory qualities ofchicken meat, indicates that the amino acidprofile of meat may be modified by dietarymeans (Imanari et al., 2008). These authorsobserved that the content of isoleucine, leucineand valine and of free glutamate as the maintaste-active component in meat was significantlyincreased by 30% when feeding diets withincreased contents of isoleucine and valine andthat this resulted in a significantly improvedsensory score of overall taste intensity.They concluded that ‘‘regulation of dietaryisoleucine and valine was more effective on freeglutamate in muscles than that of dietaryleucine’’ and that ‘‘it can be expected that thesame effects of dietary isoleucine and valine onmeat quality are applicable to other animals’’.This finding may be the basis for new research onhow to optimise sensory attributes of poultrymeat. Furthermore, this study was a first step inthe direction of a standardised description ofsensory attributes of poultry meat.

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CARCASE QUALITY

Carcase quality is important for marketing ofmeat. Many aberrations in carcase quality mayoccur during fattening and slaughtering ofpoultry. This is also the main issue in meatinspection. Suboptimal rearing conditions mayincrease the incidence of hock burns, breastblisters and injuries to the skin. Feeding dietswith high xanthophyll contents will result inyellow skin in chickens, whereas the skin colourof turkeys remains the same. Catching, grading,transporting, unloading and shackling of birdsmay cause skin haemorrhages, scratches andbroken bones. These defects can be eliminatedby optimised rearing and handling conditions. Incontrast, the slaughter process, namely thestunning of the birds, may cause carcase defectswhich cannot be easily reduced because of thegiven technical characteristics.

Electrical stunning in a water bath is thedominant technique because of its simplicity andfunctional safety, low space requirements, lowinvestment costs and easy control and mainte-nance. The main disadvantages of electricalstunning are live bird shackling, hanging ofbirds head down and the induction of muscleconvulsions. The induced spasm influences bothcarcase and meat quality (Raj et al., 1990). Rajet al. (1990), Raj and Johnson (1997) clearlydemonstrated that stunning with gas mixtures(carbon dioxide — 45% CO2þ 9% O2 in air; argon— 2% oxygenþ argon) significantly reduced theincidence of broken bones and muscle bruisingin comparison to electrical stunning in broilers(Raj et al., 1990). Authors observed the highestincidence of leg muscle bruising in electrically-stunned broilers and concluded that ‘‘this wouldimply that the shackling and/or electrical stun-ning was responsible for the bruises in the breastand legs’’ and that ‘‘this suggests that severemuscular damage rarely occurs in gaseous stun-ning’’. Comparable effects of stunning method(electrical stunning versus gaseous stunning with30% CO2, 60% argon, 10% air) on the incidenceof red pygostyle, red wing tips, haemorrhagesand broken bones (coracoid) were observed inanother study (Raj and Johnson, 1997). Theauthors stated that ‘‘the results clearly indicatedthat the incidence of broken bones (exceptfurculum) and haemorrhaging in breast musclesin association with or without the broken boneswould be substantially reduced by gas killing ofbroilers’’.

Another carcase defect which may occuroccasionally in broilers and turkeys is degenera-tive myopathy (DM). Although DM is causedbefore slaughtering it is of importance duringslaughtering as it is relevant to meat inspection.An early description of this defect was given by

Jones et al. in 1974. Degenerative myopathy ordeep pectoralis myopathy mainly occurs ‘‘in oneor both supracoracoideus muscles and is char-acterised by the appearance of a green lesion,separated from healthy muscle by connectivetissue’’. The authors assumed that, in agreementwith a previous publication on this topic ‘‘themuscle damage resulted from an impairment ofblood supply to the affected muscle’’ althoughthey did not investigate the blood vascular systemin their own study. In general, blood supply maybe the limiting factor for the viability of musclecells. Continuous selection for increased growthrate resulted in an increase of the diameter ofmuscle fibres which is particularly obvious inturkeys. This enlargement of the diameter ofmuscle fibres both increased myofibril demandfor nutrients and also increased the distancenutrients have to be transported from theendomysium to the myofibrils. Despite thisenlargement the number and size (diameter) ofblood capillaries and blood vessels remainednearly unchanged. Meanwhile, it was knownthat sudden contractions (such as violent wingflapping) or compressions (for example, fallingof heavy birds on their breasts) might cause aninterruption of blood supply, resulting in degen-erative myopathy. This defect needs to beidentified during meat inspection as it makesthe meat unfit for consumption.

MICROBIOLOGY AND PRODUCT SAFETY

Microbial contamination is a great challenge inmeat production as it may be a hazard to theconsumer. It is nearly impossible to producesterile meat as bacteria from the intestine areeasily spread over the carcase during slaughter-ing. Therefore, a strict hygiene programme hasto be applied in the slaughter plant to minimisemicrobial contamination of the meat, followingthe HACCP (Hazard Analysis of Critical ControlPoints) concept. It is clear that hygienic condi-tions on farms and during transport have to beoptimised, but this aspect will not be dealt with atthis point.

There is a wide variety of bacteria in theenvironment and in birds’ intestines, and someof them are potentially hazardous to humans.In the early nineteen seventies the occurrence ofClostridia and Pseudomonas was of major con-cern, whereas, today Salmonella andCampylobacter are the focus.

Starting in the nineteen sixties many paperson the microbial quality of poultry meat havebeen published in British Poultry Science. Workinggroups from The Queen’s University in NorthernIreland ( J.T. Patterson) and from the Universityof London (G.C. Mead) have been active in this

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field. The impact of slaughter process andtechnique was investigated in detail in 1971 byPatterson. In the synopsis of the paper Pattersonstated that ‘‘the microbial condition of poultrycarcases is shown to be influenced by thegeneral hygiene in the processing plant whichis largely determined by (i) the quality of the rawmaterials, (ii) the design of the plant andbuildings, (iii) personal hygiene, and (iv) clean-ing efficiency’’. It is clear that microbial con-tamination of raw material, that is, the birdsdelivered to slaughter, is the most critical pointas it defines the basic microbial load. However, Iwill consider the spreading of micro organismspresent during the slaughtering process and theapproaches to reduce or eliminate them. It isclear, that according to Patterson (1971) ‘‘ideallyeach processing plant should have a laboratorywith staff capable of carrying out microbial andchemical techniques’’ capable of checking theefficiency of cleaning practices and, in the caseof complaints, to give advice on solutions.During the slaughter process every point wherethe skin of the bird is breached (killing, openingof the vent, cutting neck skin, tearing of thehead with trachea and oesophagus, trimming oflegs), where equipment has direct contact to thebirds and/or meat (plucking, change of trans-port band, evisceration, lung sucker, packing)and where carcases and meat have contact withwater (scalding, interior and exterior washing,wet chilling) is critical. Cross-contamination maybe expected especially during scalding andevisceration. Contamination of equipment sur-faces and water may occur after poor cleaningand disinfection. Equipment is normally madeof either stainless steel or plastics, which are easyto clean and disinfect due to very smoothsurfaces. But mechanical load, the use ofaggressive substances during disinfection andthe use of high pressure water during cleaningmeans that over time surfaces may becomerough, allowing micro organisms to attachthemselves and hide making their eliminationmore difficult.

Strict hygiene protocols for personnel arealso very important as quite often persons arethe source of microbial contamination.Thus, personnel must wear special clothes,shoes, gloves and caps, must clean and disinfectshoes and hands before entering and leaving theslaughter facility as well as at designated intervalsduring the working day. Furthermore, staffmembers must not wear any jewellery, watchesor piercing.

Chilling of carcases is an important stage inpoultry slaughtering with regard to minimizingmicrobial load of the final product. On the onehand this stage may be a point of cross-contamination and on the other hand it may be

a point where reduction of the microbial load bywashing and disinfection is possible. For a longtime chilling in a water tank with cold or icewater was practised. Farrell and Barnes con-cluded already in 1964 that ‘‘the results given inthe paper emphasise the importance of using icewith water for chilling in poultry processingplants, so that the temperature is reduced rapidlyand kept as low as possible in the chill tanks’’.This assessment was in favour of the spin-chillerwhich was found in nearly all slaughter facilitiesfor broilers. But, Farrell and Barnes (1964)restricted their positive assessment to the pre-requisite that ‘‘the chillers are not allowed to runcontinuously throughout the day without chan-ging the slush ice’’. In general, immersionchilling has the advantage that disinfectants caneasily be added to the water. Chlorination wasassumed to be a suitable method for increasingshelf-life during water chilling. For efficientchilling Patterson (1971) recommended that thenumber of micro organisms in the final chillershould be less than 5000/ml at 22�C. Meanwhile,to improve hygienic conditions during chillingthe spin-chiller was replaced by water spraying.Today, with the change in consumers’ behaviourtowards using fresh carcases and meat forpreparing their meals, water chilling has disap-peared in slaughter houses and has beenreplaced by cold air chilling.

The question of cross-contamination duringthe slaughter process and how to control it wasanalysed in detail by Mulder et al. (1978) using anindicator micro-organism (E. coli K12). In theintroduction of their paper the authors claimedthat ‘‘by choosing the right conditions forslaughtering, and by achieving a good standardof hygiene during processing, salmonellae maybe removed from individual carcases thus avoid-ing cross-contamination of others’’, but that‘‘little is known about the incidence of cross-contamination during scalding and plucking’’.The major outcome of the study was that externalcontamination of carcases resulted in cross-contamination during scalding and plucking,whereas internal contamination resulted in fewcases of cross-contamination during plucking. Amarked reduction of externally-contaminatedcarcases (by about 1000-fold) was observedduring scalding. According to the authors, ‘‘thedecrease in numbers was due not only to highscald temperature, but also to the washing effectduring scalding’’. Thus, the final conclusion ofthis research was that, despite spreading ofmicro-organisms in some stages of the slaughterprocess, a significant reduction in carcase con-tamination can be achieved by the washing ofcarcases.

Mead et al. (1994) used the marker-organismE. coli K12 for identifying cross-contamination

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with food-borne pathogens in the slaughterprocess of standard broilers. They summarisedthe advantage of a marker organism in the waythat it ‘‘can be introduced by inoculated carcases,equipment or working surfaces at any stage in theprocess, and its transmission can be followedqualitatively and, where necessary, quantita-tively’’. In their study all critical points in theslaughter process were considered, for example,live-bird transportation, automatic killing knife,defeathering machine (plucker), head puller,conveyor for transferring carcases from slaughterline to evisceration area, metal support at exit ofvent opening machine, manual neck-skin clean-ing and inspection, metal splash-guard alongsidewater immersion chiller and water chillingsystem. The level of contamination was recordedfor neck skins, rinse samples, carcase swabs andswabs from equipment. The main outcome of thestudy was that ‘‘one of the most important stagesin hygiene control is the cleaning and disinfec-tion of transport vehicles, because these arepotential sources of contamination betweenbatches of birds and between farms’’, but thatnot all available techniques may be suitable for areduction in the microbial load. These authorsstated that ‘‘in the context of the HACCP system,it is arguable whether most of the sites ofcontamination studied are ‘‘critical controlpoints’’ or merely ‘‘control points’’. In modernpoultry processing, cross-contamination is wide-spread and occurs continuously. By reducing theproblem at as many stages as possible, however, itmay be possible to minimise the overall increasein carcases contaminated with salmonellas (forexample). Thus, the benefit from any measuretaken to limit flock infection during rearingcould be safeguarded’’. Today, commercial poul-try production and slaughtering are strictlyoperated on this principle.

In conclusion, this review highlights thenumber of comprehensive and influentialpapers in the field of poultry meat qualitypublished over the last 50 years in BritishPoultry Science. It is clear that the focus of meatquality research has evolved over the years,whereas studies of microbial quality haveremained relatively similar or increased insignificance and importance. The new EUzoonosis legislation will stimulate new researchin this field. The PSE problem in meat qualitywill be an issue for the future. In summary, theachievements of the past 50 years have resultedin major advances in poultry meat quality andsafety. Today poultry meat and poultry meatproducts are both healthy and safe, providedgood practice is followed during retailing andcooking, and contribute significantly to a healthyhuman diet.

ACKNOWLEDGEMENT

The author thanks the Editors of the Journal BritishPoultry Science for their invitation to prepare thisreview on the occasion of the 50th anniversary ofthe Journal and wishes British Poultry Science asuccessful future.

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DUNCAN, I.J.H., SLEE, G.S., KETTLEWELL, P., BERRY, P. &CARLISLE, A.J. (1986) Comparison of the stressfulness ofharvesting broiler chickens by machine and by hand.British Poultry Science, 27: 109–114.

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