How climatic changes could affect meat quality

Food Research International 43 (2010) 1866–1873

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How climatic changes could affect meat quality N.G. Gregory Royal Veterinary College, Hawkshead Lane, Hatfield AL9 7TA, United Kingdom

a r t i c l e

i n f o

Article history: Received 30 January 2009 Accepted 15 May 2009

Keywords: Climate change Heat stress Meat quality PSE meat High pH meat Transport Mortality Dark cutting beef

a b s t r a c t Climate change could affect meat quality in two ways. First, there are direct effects on organ and muscle metabolism during heat exposure which can persist after slaughter. For example heat stress can increase the risks of pale-soft-exudative meat in pigs and turkeys, heat shortening in broilers, dark cutting beef in cattle and dehydration in most species. Second, changes in livestock and poultry management practices in response to hazards that stem from climate change could indirectly lead to changes in meat quality. For example, changing to heat-tolerant Bos indicus cattle sire lines could lead to tougher, less juicy beef with less marbling. Also, pre-conditioning broilers to heat stress to encourage better survival during transport could lead to more variable breast meat pHult. The impacts that short term climate change could have will vary between regions. The ways the impacts are managed need to be based on experience while appreciating the range of approaches that could be used. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction 1.1. Relevant climate changes During the 20th century the Earth’s near-surface temperature rose by 0.6 °C. Approximately half of that increase occurred during the second half of the century and was largely due to greenhouse gas effects (Tett, Stott, Allen, Ingram, & Mitchell, 1999). The prediction is that near-surface temperature will rise by about 0.06 °C per decade and it will take 1000 years for mean near-surface temperature to rise by up to 6 °C. This trend has been interpreted as a move towards ‘‘global warming”, but the impression is that we will have a long wait for generalised warming to occur. However, in the short term there are other threats that are of more concern. It has been predicted that in some regions the weather will become more variable. For instance, unforced natural changes in the climate system such as El Niño, fluctuations in the thermohaline circulation, and anomalies of ocean heat content could lead to short-term regional changes that are separate from a more general warming effect (Smith et al., 2007). These could create more variable extremes in weather pattern and they may have spin-off effects on the meat and livestock industry. For example, they could lead to relocation of pigs and poultry in some regions as these industries follow the sources of inexpensive cereals. In addition, where water becomes limiting through less precipitation, there could be less dairy farming in drier zones, and so the sources of cull cow meat may also

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change or become more concentrated. Where livestock farmers try to withstand extremes in climate there will be escalation in some of the hazards for production and product quality, especially in semi arid regions which are already on the margins of viable farm or range land. This overview examines some of the hazards linked to extremes in heat plus reduced rainfall on meat quality and safety. 1.2. Predicting future changes in meat quality and safety Climate change could affect meat quality in one of two ways. There could be an effect through changing farming or abattoir practice to adapt to the climate change, and there could be a direct effect of the changing weather conditions on the animals. Examples of indirect effects include:  changing the genotype of animals by introducing more heat tolerant breeds;  holding animals outdoors instead of housing them during winter;  feeding low protein-high fat finisher rations to combat heatinduced growth suppression;  pre-conditioning animals to hot conditions so they will be better adapted to survive heat stress during transport to a processing plant. It will be difficult to assess the impact of such indirect effects and responses as they will evolve gradually in the livestock industry along with other changes in farming and abattoir practice.

N.G. Gregory / Food Research International 43 (2010) 1866–1873

Whereas, the direct effects on animals managed in conventional ways are more predictable. Table 1 attempts to integrate the direct and indirect effects as well as summarising some of the main effects given in part 2 of this review. Predicting the regional impact of future extremes in weather conditions can be based on two approaches. One approach is to examine the existing effects of extreme weather conditions on meat production and quality, and to use modelling to assess future impacts of incremental moves towards those weather patterns. For example, we know that heat contributes to live weight loss and mortality during transport to the abattoir (Hails, 1978). The temperature thresholds leading to faster weight loss and an increase in mortality can be determined using an epidemiological analyses of local data. From that, estimates of potential impacts can be made at a regional level. The other approach is to examine the effects of environmental conditions experimentally. In extreme situations both heat stress and exercise can influence muscle metabolism and meat quality (Lee, Hargus, Hagberg, & Forsythe, 1976; Ngoka & Froning, 1982). Quantitative relationships can then be used in models that apply to a sector of the industry. Both approaches are likely to be imprecise if they do not include reliable estimates of the degree and duration of the imminent weather changes. Theoretically, climate change could impact on meat safety as well as organoleptic quality. Global warming could affect microbial burdens on carcasses and meat, especially if the animals carry more enteric pathogens in their gut or on their body surface. One way of determining whether this is likely to happen is to examine whether there is presently a seasonal bias in carcass contamination. For example, higher counts of pathogens in summer would be consistent with an increased risk if in future there is generalised regional warming. In some parts of the world, there is a summertime emphasis in the number of reported human cases of diarrhoea or food poisoning that may be linked to contaminated meat (Domínguez et al., 2007; Oloya et al., 2007). In the case of poultry products, the prevalence of retail meat contaminated with Salmonella or Campylobacter can also have a summer bias (Eglezos, Dykes, Huang, Fegan, & Stuttard, 2008; Meldrum, Smith, & Wilson, 2006; Pointon et al., 2008). Whereas, there is little evidence that retail red meats have a seasonal contamination peak during the summer. Hot, dry summers can lead to problems with water quality and in extreme situations this can have impacts on meat quality. For example during dry summers, borehole water can be contaminated

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with nitrates leaching into an aquifer (Tegels Foods, personal communication). Where nitrates contaminate the water supply used in poultry spin chillers, there can be nitrosomyoglobin formation in the meat resulting in heat-stable pinkness in the cooked meat. This creates a false impression that the meat is undercooked (Maga, 1994). It is helpful to evaluate predictions with reasoning that is based on modes of action. Understanding the physiological basis for environmental effects is particularly useful. Take the following three cases. First, extreme heat provokes an adrenergic stress response. Adrenaline stimulates peripheral vasodilatation and muscle glycogenolysis, and if exposure is protracted before slaughter it could lead to high pHult and darker meat. However, in the case of sheep and broiler chickens, the acute heat stress that provokes sufficient adrenaline response to affect meat quality is very severe and is near the lethal limit (Lowe, Gregory, Fisher, & Payne, 2002; Nagle, Gregory, & Lowe, 2000). An example of this is given for broilers in Table 2. This table also indicates that adrenaline is a relatively provocative stress in terms of muscle glycogenolysis compared to heat stress. Second, if an animal is exercised and develops hyperthermia before it is slaughtered, the combination of high temperature and anaerobic metabolism leads to an early, stronger rigor. There is a risk that the meat could be tougher through a heat-shortening effect, and this can occur in heat stressed animals that do not undergo forced exercise (Table 2). In the case of pigs and turkeys the meat may also be paler in colour with more drip forming when presented as cuts (Gregory, 1998). Third, protracted high temperatures will lead to dehydration in water deprived animals and this can affect meat quality by making it darker in colour through shrinkage of the myofibres, and because of its dryness it has less weight loss during cooking (Jacob et al., 2006). In addition it can be drier and more sticky. Wet carcass syndrome has been a hazard in lamb carcasses when the animals have over-hydrated following dehydration during transport to abattoirs (Joubert, Marais, & Smith, 1985). 2. Individual species The upper critical temperatures for unacclimatized animals during transport are shown in Table 3 (Randall, 1993). These values correspond to the temperatures at which heat stress commences. More precisely, they are the temperatures at which additional

Table 1 Potential consequences of climate change. Primary change

Intermediary effects

Potential effects

Periodic warmer climate

Hotter conditions during rearing Changes in disease patterns Feeding low protein-high fat diets to counteract heat-induced inappetance Heat stress during transport and lairage Less risk of cold transport conditions Dehydration–rehydration cycle during preslaughter period Greater use of showering pre-slaughter Slower post-mortem carcass cooling

Changes in the frequency of mortality during transport and lairage, skin damage, carcass bruising, Escherichia coli contamination of carcasses, meat marbling, muscle myoglobin content, high pHult meat, heat shortening, dark cutting beef (DCB), dark firm dry pork, pale-softexudative (PSE) meat, meat drip, cooking loss from meat, wet carcass syndrome

Overall lower rainfall

Suitability for slaughter determined by pasture availability instead of body fatness More dry feeding before slaughter Less water available for processing plants

Changes in carcass leanness, gut microflora at slaughter, carcass chilling methods

Occasional extremes in weather conditions

Use of novel feedstuffs during natural disasters Natural disasters causing periodic large scale slaughter Droughts leading to emaciation

Changes in carcass finish and fatness, cycles of reduced livestock availability

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N.G. Gregory / Food Research International 43 (2010) 1866–1873

Table 2 Effect of pre-slaughter heat stress or adrenaline on broiler meat quality.

Body temperature at slaughter (°C) Breast meat pHult Cooked thigh L value Thigh cooking loss (%) Cooked breast shear value (kg) Plasma adrenaline just before slaughter (ng/ml) Plasma noradrenaline just before slaughter (ng/ml)

Control

Heat stress 30–35 °C for 2.5 h before slaughter

Adrenaline 1.5 mg/kg 6 h before slaughter

41.4a 5.69a 63.7a 12.0a 1.43a 1.4b 4.0a

45.1b 5.66a 61.7ab 13.0a 2.28b 2.3b 4.4a

41.5a 6.45b 60.7b 7.0b 1.66a 8.8a 2.7a

Nagle et al. (2000). Means in a row without a common superscript letter were different at p < 0.05.

Table 3 Maximum temperatures during transport in animals unacclimatized to hot conditions before they undergo raised energy expenditure in dissipating heat. Animal type

Maximum temperature (°C)

Cattle Calves Sheep – shorn Sheep – unshorn Pigs

20 25 40 25 31

Randall (1993).

energy is expended in an effort to dissipate body heat. The values will be higher than the ones shown in the table in animals accustomed to high ambient temperatures. In addition, they will be lower when humidity is high, as humid conditions limit evaporative heat loss. They serve as useful reference values when evaluating the severity of heat stress on transport mortality and meat quality. 2.1. Pigs 2.1.1. Pig mortality In temperate climates, pig deaths during transport and in lairage pens often increase when ambient temperatures rise (Barton, 1971; Smith & Allen, 1976; Warriss & Brown, 1994). High loading densities during transport make an additional contribution to the DOA (dead on arrival) rate under hot conditions (Lendfers, 1971). In northern Europe, the DOA and dead in pen (DIP) rates start to increase during May, peak in July and fall to wintertime levels in November. The number of DOAs plus DIPs is small when daytime temperature is less than 10 °C, but rises rapidly when temperature exceeds 17 °C. Beyond this point, mortality rate accelerates with temperature, and at 23.5 °C it is 6-fold higher than at 4.5 °C (Smith & Allen, 1976). One would expect the risk period to be longer when summers are longer, and summertime peak mortalities to be higher during extremes in summer heat. Muscle temperature is elevated in pigs that survive the journey and have to be emergency-slaughtered on arrival at the abattoir because they are in a heat stress crisis. In these cases rigor mortis sets in earlier or is more severe (Devloo, Geerts, & Symoens, 1971). 2.1.2. Pigmeat safety In some countries, the frequency of carcass contamination with Salmonella has been shown to be highest during the early part of summer (McDowell, Porter, Madden, Cooper, & Neill, 2007). This has not been obvious in all countries and so it would be unrealistic to generalise that the risk of Salmonella burdens on pig carcasses is likely to rise with climate change (Benschop, Stevenson, Dahl, Morris, & French, 2008). However, heat stress can increase the frequency of carcass contamination. The upper intestinal tract can act as a reservoir for particular strains of antibiotic-resistant bacteria. In pigs that had a population of ampicillin and tetracycline

resistant Escherichia coli in their ileum and caecum, heat stress before slaughter (34 °C for 8 h or longer) increased the numbers of these bacteria in the faeces and on the surface of the carcass (Moro, Beran, Griffith, & Hoffman, 2000). The heat stress increased gastrointestinal motility, causing more live antibiotic-resistant E. coli to appear in the faeces. 2.1.3. Pigmeat quality One way pig farmers could manage summertime inappetance in pigs is to decrease the crude protein content of the finisher ration and feed higher levels of fat. This should help to offset heat-induced suppression of growth rate, and reduce the cost of the ration. When 8% dietary fat was used in this way, in place of 1% fat, the meat was darker in colour and this darkness persisted during retail display or when vacuum packed (Spencer, Gaines, Berg, & Allee, 2005). The early scientific literature on the effects of long term controlled environmental temperatures and humidity on pigmeat quality have been reviewed by Judge (1968). Unfortunately, most of that work was done in pigs stunned by captive bolt, and this predisposed them to developing paler meat from carcass convulsions. Nevertheless, Poland China pigs reared from weaning to slaughter in alternating high and low environmental temperatures (repeated cycles of 3 days at 29 °C followed by 3 days 18 °C, both at 30% RH) developed paler meat compared to being reared at constant 18 or 29 °C at 30% RH. High humidities (85% RH) resulted in darker meat regardless of temperature, and they had more effect than alternating humidities (85% and 30% RH) in Landrace pigs. The rearing temperature effects on meat colour were not due to any difference in muscle temperature at slaughter. Instead, there was a difference in the metabolic capacity of the muscle which was due to a shift towards anaerobic muscle fibre types containing less myoglobin in pigs reared under alternating temperatures at moderate humidity. In Danish Landrace pigs, summer conditions have been associated with paler meat colour compared with wintertime (Barton, 1971; Jonsson, 1968). The poorer quality was not due to marked differences in the proportion of pigs developing PSE. Instead, it was due to more severe cases of PSE (Table 4). In Brazil, transport during summer conditions (15–35 °C) has been associated with less skin bruising compared to wintertime (0–31 °C) (dalla Costa et al., 2007). It was suggested that in winter there was more huddling together in the truck as well as more activity. The meat was also darker. In pigs that were predominantly stress sensitive heterozygotes, heat stress in lairage lasting up to 3 h had pronounced effects on meat quality (Santos et al., 1997). The frequency of PSE carcasses rose from 38% when the lairage was 12 °C/90% RH, to 47% at 20 °C/90% RH and 58% at 35 °C/85% RH. In severe conditions, prompt slaughter on arrival had some advantages, as the longer the exposure to heat stress plus high humidity the higher the prevalence of PSE meat.

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N.G. Gregory / Food Research International 43 (2010) 1866–1873 Table 4 Frequency of PSE pig carcasses during three seasons of the year in Denmark (%). Season

Noon temperature (°C)

Number of pigs

Slightly PSE

PSE

Severe PSE

Total PSE

Summer Autumn Winter

25 10 <0

858 531 1228

14.5 10.7 6.4

21.7 34.5 29.2

10.4 0.9 3.3

46.5 46.1 38.9

Barton (1971).

2.2. Poultry It has been suggested that modern broiler breeds are more susceptible to heat stress than earlier genotypes. It is claimed that heat-induced suppression of growth is now being seen at lower ambient temperatures in commercial strains (Deeb, Shlosberg, & Cahaner, 2002). In addition, fast growing strains have lower survival during heat stress (Yalcin, Õzkan, Türkmul´, & Siegel, 2001). Heat stress suppresses appetite, but this can be controlled by increasing air velocity in the shed with the fans. Under Israeli conditions, when there is a high risk of heat stress in the grower sheds (35 °C, 60% RH), the optimum air velocity is 1.5–2.0 m/s (Yahav, Straschnow, Vax, Razakovski, & Shinder, 2001). Weight loss can occur during the pre-slaughter period when birds are deprived of feed and water. Protecting birds from heat stress during this period can help control some of that weight loss (Benibo & Farr, 1985). 2.2.1. Broiler mortality In northern Europe, death during transport increases when maximum daily temperature in the shade rises above 17 °C (Warriss, Pagazaurtundna, & Brown, 2005). For the UK, this corresponds to early summer, when the elevated DOA rate lasts for about three months. Losses can be minimised by stocking the transport crates less densely during hot conditions, and cooling the birds with fans or sprinklers on arrival at the processing plant. Preconditioning broilers during their growing period to hot episodes can enhance survival to subsequent heat stress before slaughter. However, it does not have any beneficial effect on water retention in the meat following slaughter. In situations where heat stress is not encountered during the pre-slaughter period, cooking loss from breast and leg meat is greater (Northcutt, Foegeding, & Edens, 1994). One way of controlling leg disorders in fast growing broiler strains is to briefly reduce their growth during the first or second week after hatching, and allow them to catch up during the remainder of the growing period. This also helps to reduce their subsequent susceptibility to heat stress (38 °C for 2 h per day for 7 days) (Table 5; Zulkifli, Che Norma, Israf, & Omar, 2000). 2.2.2. Poultry meat safety Work in Australia has indicated that retail products are more likely to carry higher total viable bacteria counts in summer. E. coli numbers can also be raised depending on the type of product

and how it is managed (Eglezos et al., 2008; Pointon et al., 2008). It has been suggested that the cause of seasonal increases in contamination could include physiological features in the live bird. However, the evidence does not entirely support that view. Heat stress in broilers does not appear to have a consistent effect in promoting shedding of Salmonella spp. in the faeces of pre-conditioned (29– 32 °C for 8 h per day for 7 days) 5-week old birds (Traub-Dargatz, Ladely, Dargatz, & Fedorka-Cray, 2006). In addition, experience in the US has shown that it is often more difficult to infect chicks experimentally with Salmonella enteritidis when they have been hatched in the late-summer months compared with other times of the year (Farnell, Moore, McElroy, Hargis, & Caldwell, 2001). If there is a genuine seasonal physiological effect, the mechanism is obscure. 2.2.3. Poultry meat quality The effects of acute heat stress need to be examined separately from lifetime exposure to hot conditions, when considering the precise causes of a warmer climate on poultry meat quality. The genotype of the bird may also need to be considered. When a commercial strain of broiler (Ross) was grown from 14 days of age to slaughter at a high temperature (33 °C day/27 °C night), compared to 23 °C day/17 °C night time temperatures, the birds kept at the higher temperatures had higher breast meat pHult (N’dri, Mignon-Grasteau, Sellier, Beaumont, & Tixier-Boichard, 2007). Paradoxically, a separate study showed that Ross birds had a lower pHult when reared at high temperatures, and this was associated with a paler, less red breast meat (Aksßit, Yalçin, Özkan, Metin, & Özdemir, 2006). Asian Arbor Acres birds seem to be less affected. Although heat stress during their growing period (34 °C from 5 to 8 weeks of age) can affect growth rate and carcass yield, it probably has limited effect on meat quality independent of its effect on appetite (Lu, Wen, & Zhang, 2007). The heat-induced suppression of appetite explained the differences in objective measures of paleness and drip formation (Table 6). In turkey toms, heat stress (38/32 °C vs. 24/16 °C, day/night) during the last 5 weeks of the rearing period, resulted in lower breast meat pH15 min and pHult, and paler meat with greater drip and cooking loss (McKee & Sams, 1997). In other words, the same features as PSE meat were found. When the PSE condition does not develop, acute heat stress (42 °C for 1 h before slaughter) can make breast meat tougher and redder (Froning, Babji, & Mather, 1978). In broilers that have not been pre-conditioned, acute heat stress (34–41 °C for 1–18 h) can lower thigh meat pHult, and superoxide

Table 5 Effect of early growth restriction on subsequent susceptibility to heat stress. Feed restriction during 4–6 days

Live weight for age at 42 days Feed conversion ratio (g/g) Mortality % during heat challenge Heterophil-lymphocyte ratio after the heat challenge

Ad libitum

80% ad libitum

60% ad libitum

40% ad libitum

1.852a 2.00 17a 0.76a

1.847b 1.93 10a 0.73a

1.921a 1.93 0b 0.57b

1.828b 1.89 5b 0.66ab

Zulkifli et al. (2000). Means in a row without a common superscript letter were different at p < 0.05.

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Table 6 Effect of heat stress for 3 weeks before slaughter on growth, carcass and meat quality in broilers. 21 °C/ad libitum Feed intake (5–8 weeks) (g/day) Final live weight (kg) Weight gain (g/day) Feed to gain ratio Mortality (%) Breast (g/100 g live weight) Leg (g/100 g live weight) Abdominal fat (g/100 g live weight) Subcutaneous fat (g/100 g live weight) Intermuscular fat (g/100 g live weight) Carcass weight (g/100 g live weight) Breast meat pH15 min Breast meat pHult Breast L value Breast a value Breast drip loss Breast shear force (kg)

169.9 ± 7.9a 2619 ± 111a 61 ± 5a 2.8 ± 0.2b 8a 16.96 ± 0.34a 25.27 ± 0.44b 1.57 ± 0.23a 13.76 ± 1.33a 0.43 ± 0.05a 73.36 ± 0.72b 6.08 ± 0.08a 6.00 ± 0.10ab 45.08 ± 1.00b 8.67 ± 0.71 1.56 ± 0.23b 1.17 ± 0.22

21 °C/pair-fedA b

94.0 ± 4.5 1962 ± 89b 29 ± 5b 3.2 ± 0.4ab 5a 16.88 ± 1.00ab 25.33 ± 1.46b 0.75 ± 0.10b 10.96 ± 0.72b 0.22 ± 0.02c 73.89 ± 0.85b 5.95 ± 0.07b 5.90 ± 0.06b 45.79 ± 0.70ab 9.87 ± 1.17 3.04 ± 0.97a 1.57 ± 0.49

34 °C/ad libitum 93.6 ± 4.8b 1876 ± 92b 22 ± 4c 3.9 ± 0.8a 36b 15.99 ± 0.65b 26.61 ± 0.83a 1.35 ± 0.19a 11.08 ± 0.98b 0.35 ± 0.04b 75.27 ± 0.89a 6.15 ± 0.09a 6.09 ± 0.09a 47.05 ± 2.02a 8.89 ± 2.98 2.41 ± 0.27a 1.33 ± 0.14

Lu et al. (2007). Means in a row without a common superscript letter were different at p < 0.05. A Pair-fed with the 34 °C/ad libitum group.

producing capacity by mitochondria in breast muscle can be raised. Drip loss from breast meat and cooking loss from leg meat can also be higher (Debut et al., 2003; Mujahid, Akiba, & Toyomizu, 2007; Northcutt et al., 1994; Petracci, Fletcher, & Northcutt, 2001). Some, but not all studies have shown that breast meat can be tougher following pre-slaughter heat stress, or that it may develop a stronger rigor (Lee et al., 1976; Wood & Richards, 1975). There has been no consistent effect on breast meat a value when considering all the experiments, and no effect has been seen on heat-stable pinkness (Nagle, et al., 2000). When acute heat stress (35 °C for 3.5 h) was compared with the stress produced by longer than usual shackling (2 min compared to 10 s), heat stress was no worse than long shackling and it did not have an additive deleterious effect on meat quality (Berri et al., 2005). Skin tears and muscle damage during plucking are more common during warmer months, especially in kosher slaughtered broilers which are not scalded to loosen the feathers. The effect is probably due to weaker skin in birds grown during the warmer season (Pitcovski, Pinchasov, Meron, & Malka, 1994). To summarise, most of the evidence points towards a greater risk of the PSE condition in poultry that experience acute heat stress before slaughter. 2.3. Sheep and cattle 2.3.1. Mortality Deaths during transport are relatively uncommon in ruminants, but there have been isolated reports from New Zealand of heat stress-related deaths in red deer during transport and in sheep held in a vehicle parked in the sun (personal observations). There have also been cases of high DOA rates in semi-feral rangeland cattle in the north of Australia (McQueen, 1972). There was one instance when 19 out of 35 cattle arrived dead at the abattoir after a 640 km journey. Those that survived and were in extremis were promptly slaughtered, and were passed as fit for human consumption at meat inspection. 2.3.2. Meat safety In ruminants, the seasonal veterinary public health risks vary with each pathogen and according to whether the stock are raised indoors or outdoors. Keeping livestock outdoors can increase the risk of endoparasites. However, it should reduce the risk of acquir-

ing viable pathogenic gut microorganisms, provided stocking densities are low and faeces are exposed to the desiccating and the direct effects of ultraviolet radiation from the sun. Keeping calves outdoors all the year round could favour enteric Cryptosporidia (Kvácˇ, Kouba, & Vítovec, 2006). In temperate wet climates of New Zealand, Campylobacter numbers in cattle dung pats tend to be highest as temperatures rise during spring (Moriarty, Sinton, Mackenzie, Karki, & Wood, 2008). Whereas in a range of climates there is no consistent seasonal effect in the shedding of faecal E. coli O157:H7 by cattle, which suggests that climate change may not increase the risk of cross-contamination with this particular pathogen (Alam & Zurek, 2006). There can be more pronounced faecal shedding of paratuberculosis Mycobacteria and less Salmonella in winter (Crossley, Zagmutt-Vergara, Fycock, Whitlock, & Gardner, 2005; Fossler et al., 2005). Under hot conditions it is good practice to sprinkle feedlot cattle with water to alleviate heat stress and control aerial dust. In a study in southern US, daily sprinkling for 2 min every hour between 11.00 and 17.00 h when ambient temperature exceeded 30 °C, did not increase the prevalence of Salmonella or E. coli O157:H7 in faeces or on the hides (Morrow et al., 2005). A key issue is the level of contamination on the carcasses leaving the abattoirs. The proportion of Salmonella positive carcasses was shown to be high during summer (Ruby, Zhu, & Ingham, 2007). The reasons underpinning this seasonal effect were not established. 2.3.3. Meat quality In cattle, high ambient temperatures can favour greater muscle marbling and fat deposition in internal depots, in place of the subcutaneous depot (Mader & Davis 2004; Nardone, Ronchi, Lacetera, & Bernabuci, 2006). This could be an advantage for some specialised markets. However, high ambient temperatures can also lead to more dark cutting beef. This has been seen in both the US and the Oman. In the Oman, the proportion of dark cutters (pHult > 6.0) rose to almost 60% when mean daily temperature was 35 °C (Kadim et al., 2004). In four states of the US, where the overall frequency of dark cutters was substantially less, it was highest during the second half of summer (Fig. 1; Kreikemeier, Unruh, & Eck, 1998). Providing shade in a feedlot can reduce the frequency of dark cutters (Mitlöhner, Galyean, & McGlone, 2002). Jacobson et al. (1997) examined the relationships between preslaughter body temperature and pHult in 159 cattle. A high pHult was associated with elevated rectal temperature immediately

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% Dark cutters

1.6

(Wheeler, Cundiff, Shakelford, & Koohmaraie, 2001). The toughness can be avoided either by limiting the proportion of B. indicus in the slaughter generation composites, by increasing the post-mortem aging period in the abattoir, or by using a heat adapted Bos Taurus breed such as the Tuli instead of Brahman. Tuli-sired cattle also deposit fat internally instead of in the carcass which may be an advantage for both table and manufactured meat markets (Sprinkle et al., 1998).

1.4 1.2 1 0.8 0.6 0.4 0.2 0 1

3

5

7

9

11

Month of year Fig. 1. Frequency of dark cutting beef carcasses according to month of the year in US (Kreikemeier et al., 1998).

before slaughter in over half the animals. They put forward the explanation that many cattle developed hyperthermia shortly before slaughter but in some the response to glycogenolytic stress was not long enough to result in dark cutting beef even though it had been sufficient to raise body temperature (Fig. 2). Heat tolerance can be improved by introducing tropicallyadapted composite breeds such as Bos indicus Brahman crosses, but it will lead to tougher meat through raised calpastatin activity in the meat (O’Connor, Tatum, Wulf, Green, & Smith, 1997). Brahman crosses also have less marbling and reduced meat juiciness

2.4. Other species In rabbits grown during a Mediterranean summer, a short (1 h) journey before slaughter resulted in less risk of the dark firm dry condition compared with rabbits grown in winter (Table 7). However, longer journeys (7 h) during summer resulted in slightly tougher loin meat, presumably from a post-mortem heat-shortening effect (María et al., 2006). In fish farming, warm conditions favour the formation of earthy taints in freshwater by cyanobacteria. These occur as off-flavours in fishmeat and are usually due to lipophilic compounds 2methyl-isoborneol and geosmin. The likelihood of taints in fish grown in contaminated water is higher during warm conditions (Robertson, Hammond, Jauncey, Beveridge, & Lawton, 2006). Depuration rate (the rate at which off-flavours can be purged from the fish) may also be influenced by water temperature.

Fig. 2. Diagramatic representation of body temperature profiles for individual cattle destined to produce different pHult meat, from the start of pre-slaughter stress up to the time each animal is slaughtered (Jacobson et al., 1997).

Table 7 Effect of season and journey duration on rabbit meat quality. Loin meat quality parameter ± se

Journey duration Summer (28 °CA)

pH24h Water holding capacity Toughness (kgf/cm2) Colour L value Colour a value

Winter (11 °CA)

1h

7h

1h

7h

5.75 ± 0.02a 12.6 ± 0.5a 0.25 ± 0.01a 58.5 ± 0.3ab 2.34 ± 0.21a

5.77 ± 0.01a 12.1 ± 0.4a 0.31 ± 0.02b 59.4 ± 0.4b 2.49 ± 0.20a

5.97 ± 0.03b 14.9 ± 0.5b 0.42 ± 0.02c 58.4 ± 0.3ab 3.45 ± 0.22b

5.90 ± 0.02b 14.6 ± 0.4b 0.31 ± 0.02b 58.0 ± 0.3a 4.19 ± 0.26c

Means with a different superscript letter in a row indicate significant differences at p < 0.05. María et al. (2006). A Average outside temperature.

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3. Conclusions Extremes in summertime temperatures increase the risk of DOAs, and the risk of PSE meat in pigs and turkeys, as well as dark cutting beef in cattle. Some of these effects may be avoided by preemptive or reactive measures such as changing the genotype or introducing better methods of cooling animals before slaughter. However, changing to heat tolerant cattle genotypes could introduce other meat quality problems, such as toughness from B. indicus breeds. The potential hazards from rising environmental temperatures on meat safety will depend on local circumstances. There are concerns, based on normal season effects, that rising environmental temperatures will pose a greater risk of meat spoilage and carcass contamination with E. coli in poultry and Salmonella in a range of species. 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