The current review seeks to highlight the concerns that have been raised on pre-slaughter stress, contributing factors and its consequent effects on cattle behavioural responses and the quality of beef; inter-linking the activities involved from birth to slaughter. Such information is crucial in light of the consumer concerns on overall animal welfare, quality of meat and food security. Slaughter animals are exposed to different conditions during production and transportation to abattoirs on a daily basis. However; the majority of studies that have been done previously singled out different environments in the meat production chain, while conclusions have been made that the welfare of slaughter animals and the quality of meat harvested from them is dependent on the whole chain. Behaviour is a critical component used to evaluate the animals’ wellbeing and it has been reported to have an effect on product quality. Apart from the influence of on-farm, transportation and abattoir conditions, the genetic background of the animal also affects how it perceives and responds to certain encounters. Stress activates the animals’ hypothalamic-pituitary-adrenal activity, triggering release of various stress hormones such as catecholamines and cortisol, thus glycogen depletion prior slaughter, elevated ultimate pH and poor muscle-meat conversion. Pre-slaughter stress sometimes results to cattle attaining bruises, resulting to the affected parts of the carcass being trimmed and condemned for human consumption, downgrading of the carcass and thus profit losses.
According to Boissy and Erhard , animal welfare is a result of how animals identify with their surroundings and previous experiences. Different environments in the meat production chain, the factors around them and their effects on animal welfare and beef production have been reported in recent research outputs and reviews. Specifically, Waiblinger et al  looked at the interaction between humans and animals at the farm, concluding that it is a significant factor to consider in improving the welfare of farmed animals and the stockpersons. Good stockmanship has been reported to improve productivity , and this kind of treatment should begin at early stages of life [4,5].
However, Ndou et al  highlighted that animal welfare and its further effects on product quality are highly considered in developed countries than the developing ones. They further hinted on the on-farm multipurpose cattle production systems and their consequences on beef quality. Work has been done on animal transportation conditions and their effects on animal welfare and meat quality [7,8], while Grandin  covered different livestock welfare issues at the farm and abattoirs, further relating them to consumer concerns. Moreover, Vimiso et al  reported that the African perspective on meat production and quality, particularly of the rural consumers have received little attention from the research areas.
All these issues in the meat production system have been separately covered without encompassing the whole production chain. However, the series of processes involved in meat production begins at the farm where animals are born, reared, fattened, transported to the slaughter-house, slaughtered and then converted to meat to be distributed to consumers through retailers. Miranda-de la Lama et al  described this phenomenon as the meat supply chain. Some studies that have been independently conducted on each of these events; predominantly the pre-slaughter occasions and they proved to induce stress to slaughter animals [11–17].
Some parts of the developed world have done a lot to develop measures to improve the animals’ livelihood, together with ensuring good quality animal products for the consumers. However, some parts of the developing world such as Africa have been dragging behind due to several factors such as traditional customs and beliefs practised by different ethnic groups . To ensure maximum product quality, this knowledge should be of importance to everyone in the production chain; from the stockman, farmer, transporter, abattoir worker, and the designers of animal facilities . Therefore; knowledge of animal stress inducers, animal response-behaviour and its subsequent effects on meat product quality is of importance to ensure an efficient and economic enterprise.
What happens when an animal is exposed to change?
In trying to cope with a given situation, animals exhibit behavioural changes (Table 1), which can either be “positive” or “negative” and can be used as apparent animal welfare indicators [18,19]. The positive reflect normal and desirable behaviour; while the negative is a diversion from the normal. These behavioural changes can also be reflected through biochemical changes in the animal (Figure 1). Environmental unsettle activates the animals’ hypothalamic-pituitary-adrenal activity due to fear , thus leading to some biochemical changes . Various stressors result to release of stress hormones such as catecholamines and cortisol, resulting to glycogen depletion prior slaughter, elevated ultimate pH and unacceptable conversion from muscle to meat [16,21]. Furthermore, Bourguet et al  observed that exercise and psychological stress just before slaughter increases muscle metabolic activity, which may continue after death, resulting in faster post-mortem pH decline and thus decreased meat quality .
Moreover, previous animal-human interaction relationships have been reported to be an influential factor and a determinant of how animals will perceive pre-slaughter exposure at a later stage. Boissy  reported that animals often perceive contact with a human being as a predatory encounter, to such an extent that they would panic and try to avoid human beings out of fear. Fear of humans by cattle can thus compromise animal welfare prior to slaughter, resulting in reduced productivity of quality meat . However, good stockmanship at the farm is said to improve this problem such that animals are familiar with handling even prior to slaughter. In contrast, removal of animals from one environment to another for the purpose of slaughter has a potential to alter this perception.
Miranda-de la Lama et al  singled out transportation to be the link between all the activities that take place before slaughter. It has been found to greatly contribute to pre-slaughter stress [8,14,25–27]. Additionally, the effects of speed at which the transportation vehicle travels, the design of the vehicle (size, space, surface) and the stocking density during transportation were observed to contribute greatly to pre-slaughter stress . Broom and Fraser  reported that lack of control in the animals’ environment may result in strange behaviours in trying to adjust to physiological changes.
In addition, the abattoir environment offers the animals a new and different experience to that of the farm, with more confined structures and interactions thus behavioural and physiological adjustments required to get comfortable. Researchers have evaluated lairage conditions, slaughter processes-with or without stunning, bleed-out times and positions, duration between stunning and exsanguination together with their effects on animal welfare and meat quality [6,28–39]. Nevertheless, animal age, gender, breed, and species also play a role in the way animals individually respond to stress thus production [15,24,40–42].
The impact of the animals’ background and characteristics on welfare thus production
Across species, the main contributing factor in selecting meat producing animals has always been the ability of the animal to produce a profitable quantity of quality meat in a given time. However, continuous research has shown significant links between the animals’ response (behavioural and physiological) towards specific conditions and stimuli during the production cycle and thus the quality of meat that the animal produces. Specifically, temperamental cattle have been reported to be difficult to handle and are thus susceptible to handling stress, resulting in poor meat quality [43,44]. An in-depth understanding reveals that the animals’ intrinsic factors such as type of species, breed/genotype, age and gender contribute greatly to this perception and response [35,36,42,45] thus meat quality [15,24,40,41].
Furthermore, older animals have been reported to respond better (calm) than younger ones [35,36,46–48]. This may be due to their elongated exposure and experience, later developing some sense of tolerance. Studies on sheep reported that castrates were more relaxed and less fearful compared to ewes [35,36, 48,49] and this may be related to the differences in hormonal activities operating in the two genders. However, Dweyer  reported that male animals show more aggression, while the female species only engage in combative behaviour when competing for limited resources. Additionally, Njisane  reported that cross-bred cattle can be more temperamental compared to pure-bred cattle due to a mixture of different gene sequences, mainly aimed to producing quality meat product while the behavioural impacts may not be known. Grandin  also reported that animals that went through market-handling settle better in stressful environments like the abattoir due to similar previous experiences, compared to those sourced directly from the farm. However, it was also reported that cattle that have been market-handled through auctions tend to have more bruises than those sourced directly from farms .
On-farm exposure conditions and activities
Cattle farming has greatly contributed towards the success of the meat industry. Beef producing cattle are normally reared extensively during their early stages of life and then sometimes transferred to intensive systems during the fattening and finishing stages . This system is believed to offer good animal welfare  and is characterised by free ranging and uninterrupted time budgeting, which can be classified as “normal behaviour” of cattle. Time-budgeting is an act of performing various activities like satiating hunger or thirst  animal-animal interactions for survival and pleasure purposes. The on-farm concept has been mostly established in the dairy production system, relating it to milk production [42,55,56]. However, the meat producing sector has given it very little attention even though it has a potential to determine and produce solutions to some of the challenges experienced, like in the dairy.
On-farm human-animal interactions, including time to time managerial activities and/or routines have, however, been ventured. Good stockmanship has been reported to improve productivity through reduction of fear and promotion of easy handling [3,20]. In addition, it has been recommended that farm animals be subjected to human contact from an early age in order to accustom them to human company for better handling at a later stage [4,57,58]. However, this may be a challenge to achieve in some countries that are still using the extensive production system to produce large herds of beef cattle to supply the meat industry with enough quantities to meet consumer demands and generate profit. This concept mostly accommodates dairy farmers whose production is already day to day, the stall farming systems and small units for research purposes.
However, higher cortisol levels during restraint are likely to be found in the extensively raised and less accustomed to handling beef cattle compared to dairy cows . General human-animal interactions seen in beef farming include occasional managerial routines such as weighing, castration, dipping, branding, and vaccination, among others. Raussi  and Probst et al  reported these events to be unpleasant for animals, such that fear towards humans may be developed. Animals often recognise contact with human beings as destructive . In order to deal with situations, animals may respond and even develop certain behaviours or strategies such as avoidance or clustering in trying to cope . Furthermore, cattle and sheep can remember an aversive experience for many months after it occurs [61,62]. Therefore, the “pre-slaughter” preparation of cattle then remains an un-resolved problem.
Pre-slaughter events and their impact on animal welfare and productivity
Pre-slaughter events begin the moment animals are led and loaded on a truck/vehicle at the farm to be sent for slaughter. Ferguson and Warner  described pre-slaughter as the conditions and practices during which animals are moved at the farm through to the knocking box at the abattoir. At this stage animals are exposed to extra physical activity, way more than normal animal-human interaction and multiple unfamiliar persons. Grandin  reported that situations unfamiliar to the animals such as transport, pre-slaughter treatment and handling at the abattoir, can be extremely stressful to beef cattle. In addition, the abrupt change in their social or physical settings exacerbates trauma [7,13,63].
Miranda-de la Lama et al  described transportation as the key component joining the events involved in the pre-slaughter logistics chain. This process is largely an exceptionally stressful event in the animals’ life [7,64]. It often involves novel and tense exposures such as crowding, noisy vehicles without access to food and water or space to rest, pre-transport management, vibrations, social regrouping, restraint, loading and unloading, transportation duration and climatic factors [65–68]. However, the extent of animal welfare alteration and what can be measured as positive or negative behaviour, if there is any, during this stage has not been clearly defined.
Tarrant et al  reported that inability to move and face the preferred direction during transportation caused cattle to lose balance and even fall. However, maintaining balance in a moving vehicle, which is a new experience, while standing and sometimes with little space to move may be hard to achieve. It was also reported that long transportation hours in poor condition transportation vehicles may be unfavourable to animal welfare ; while it has also been pointed out that prolonged experience of the same stressor results in familiarity [69–72]. However, Mota-Rojas et al  reported that transportation to the abattoir should not take more than 16 hours.
Pre-slaughter stress during transportation has also been reported to influence the immune responses of cattle , which may result in the release of stress hormones . Moreover, transportation at high stocking density (above 550 kg/m2) was reported to elevate plasma cortisol [26,75,76]. However; validation of these points through blood or urine extraction for hormonal analysis is questionable. The stress hormones surge in these samples may be due to handling or the novel environment (vehicle of arrival at abattoir) during the sampling. Nevertheless, ensuring good transportation is not only of animal welfare and meat quality importance, it is also of economic importance .
Abattoir conditions and their impacts
Miranda-de la Lama et al  described the abattoir design as generally based on conventional architectural criteria, such as space optimization or how to facilitate human movement, and not on the behavioural characteristics of the animals. As opposed to the green grass at the farm, abattoirs are mainly concrete and “unnatural”. The animal perception and response to the adverse conditions at the abattoir depend on its background and previous experience [13,43]. However, animal response behaviour can also be influenced by unfamiliar environments such as concreted abattoir, many abattoir workers  and other animals from different farms and of other species [7,63]. For instance, cattle may struggle to adapt with the loud squealing sounds made by pigs during lairaging. Moreover, McGreevy  stated that the loud noise at the abattoir affects the animals’ response, as opposed to the quiet environment at the farm.
Grandin  also reported that cattle perceive the abattoir environment in the same way as at the farm during procedures like vaccination and other managerial processes that involve moving animals through the race. However, there is need to clearly classify to what extant can this be expressed. Vimiso et al  reported that animal handling differs between the farm and the abattoir. In addition to that, animals would have been exposed to extensive stressors pre-slaughter compared to just farm managerial procedures. The presence of physical distractions (e.g. shiny objects, dangling chains), humans, and change of either dark or light in the race frightens the animal, resulting in anxiety [22,80]. However, it was indicated that the animals are not aware that they will die at the abattoir . Grandin [28,29] also reported that use of electric prods, slipping in the stunning box, and missed stuns, sharp edges on equipment or excessive pressure from a restraint device encourages vocalization in beef cattle at the abattoir.
The impact on the quality of meat
Pre-slaughter handling stress does not only affect the welfare of the animals, but also to a greater extent has an impact on the quality of meat produced from animals of different species [7,15,16,20,81,82]. Lawrie  recounted that the quality of meat is highly affected by behavioural and physiological response of the animal before slaughter. Pre-slaughter handling affects meat quality attributes, such as colour, pH and texture [15,16, 81,84]. Stress-related behavioural and physiological changes have been reported to reduce the quality of meat [85,86] through glycogen depletion and elevated ultimate pH [16,21,87].
Rapid depletion of muscle glycogen during handling, transportation, pre-and post-slaughter results to low lactic acid production; thus dark, firm, and dry meat produced . Glucose in the blood and glycogen in the muscle promotes glycolysis, and thus the formation of lactic acid  resulting in tougher meat with higher cooking losses [90,91]. Furthermore, Gajana et al  reported that longer transportation time and higher stocking density significantly affected pHu and thus reduced meat quality. Warner et al  related dark cutting in beef with the time spent in lairage pre-slaughter. While the animal’s genetic background and its exposure prior to slaughter determines its behavioural and physiological responses when encountered with stressful situations, this also has an implication on muscle metabolism .
Temperamental cattle such as cross-bred steers can be difficult to handle and have an increased responsiveness to stressors; consequently exhibit avoidance behaviour and elevated catecholamine, cortisol and Creatine Kinase [43,44,51,94,95]. Furthermore, such animals are more prone to injuries, also referred to as bruising. Strappini et al  described bruises as subcutaneous lesions found on a carcass after skinning, during the dressing process. Bruised cattle produce unacceptably higher muscle pH (>6.0), faster glycogen depletion, muscle darkening, toughening and poor meat shelf-life [16,95,97]. Bruising is of economic importance and may result to profit losses due to the bruised parts of the carcass being condemned for human consumption, as well the bruised carcasses being downgraded.
Consumer concerns, laws and regulations governing meat production in the developing world
The developing world such as Africa shows a lot of potential in meat production and export exchange, particularly for beef, due to its ability and resources to accommodate and nurture both indigenous and exotic cattle breeds. Scholtz et al  reported that the climatic and agricultural conditions in this part of the world allow for many areas of compatible interest and opportunities, regarding beef cattle production. Bello et al  reported that there has been an information gap between the developing and the developed world. Even so, it is also important to realise the geographical, climatic and systematic differences of the two worlds. Therefore, there is need to intensify research in this regard and come up with findings that are suitable and complement the developing world conditions.
Despite the laws and regulations that govern food animals , meat production  and consumption, Ndou et al  described the developing world as giving low priority to the welfare of animals due to factors such as traditional customs and beliefs, lack of knowledge in animal handling and sub-standard handling facilities. This may then make it hard for these countries to compete with the rest of the world due to high prevalence of food insecurity and poverty , thus intensifying socio-economic challenges and constraints . Furthermore; the elevated concerns from consumers on how the animal was treated before it was slaughtered as well as how it was processed (hygiene) affect the way they perceive meat .
Bello et al  discovered that some abattoirs in Nigeria neglect the practice of regular ante-mortem and post-mortem inspection of slaughter animals, conventional sanitation practices in operation and post-operation cycle thus putting public health in jeopardy due to unsafe meat production. They also reported that these shortcomings threatened achievement of sustainable food safety. Furthermore, Font-I-Furnols et al  reported that meat consumers were more concerned of the product’s place of origin than its price or the feed the animal took; and they were more comfortable with locally produced meat. However, a study in South Africa revealed that rural consumers were more concerned about the price of the product than any other factor . The current status of the developing world regarding animal welfare awareness and meat quality concerns puts it on the edge relating to import and export participation with the rest of the world through the meat industry in improving the economy. Ferguson et al  concluded in a review that the industry should pay attention and even respond to the consumer and societal demands for more sustainable and ethical animal farming systems and practices.
Some possible measures to adjust in order to improve animal welfare and meat quality production
Through some trials done to investigate the pre and post slaughter exhibition, conclusions and recommendations have been reported in trying to minimise pre-slaughter stress and thus improve meat quality [8,11,15,16,29]. In addition, Chulayo and Muchenje  reported that to ensure good production, animal welfare should be prioritized in all production sectors; on the farm, during transportation and at the abattoir. Some recommendations that have been drafted are described in Table 2.
Knowledge empowerment and enforcement
Through further research on the gaps identified in this paper, more knowledge generated can be of great addition. Furthermore, ease of information transformation from researchers to farmers in an understandable and simple manner still requires establishing. Methods like regular workshops, magazine articles, blogging and social networks may assist. Sequentially, this knowledge may be easily imparted to the stockman and everyone else involved in animal handling in both farms and abattoirs. To ensure maximum product quality and economic returns, everyone in the production chain (the stockman, farmer, transporter, abattoir worker, the designers of animal facilities and consumers) must be well-informed of animal welfare and its subsequent effects on meat product quality .
Merging farms with abattoirs
In addition, to eliminate the pre-slaughter transportation stress, bringing the fattening/feedlot facilities closer to the slaughter house (Figure 2) may improve the situation. Animals can be transported to these facilities at least 2 to 3 months prior the slaughter date such that herding them by foot to the abattoir would be possible. The abattoirs may adopt this either individually or co-joined with their regular suppliers. This could be viewed as an investment because installation would be a once off cost with long term benefits. Though literature has reported that cattle prefer extensive conditions over confinement [53,105,106], this has a potential to improve animal adaptation to the abattoir workers, surrounding conditions, as well as increasing profit in the long run. A similar scenario can be observed in pasture-based dairy farms, where animals are hoofed for 1 to 3 km to the milking parlour once or twice a day for milking. Some abattoirs in South Africa already have farms where they fatten their constant supply of beef cattle. However, just like privately owned farms, they are situated remotely from the abattoir and thus require the use of transportation vehicles to move animals before slaughter. Though feedloting was reported to be unfriendly towards animal welfare due to confinement , Vimiso and Muchenje  reported that animals that were hoofed to the abattoir had lower bruising scores compared to those that were transported either directly from the farm or through auctions.
Technology advancement in abattoirs
Livestock of all species often react and refuse to move in the handling facilities due to stress and anxiety if they spot a distraction or are separated from their groups [22,43,80]. However, as opposed to using electric probes to motivate animal movement, upgrading and use of automated machinery to convey animals might be helpful. Some commercial abattoirs use conveyer restrainers for pigs and sheep [35,36], which reduce strain on both animals and handlers during heading. Furthermore, Gregory  reported that for effective and animal welfare friendly results, it is important to understand the causes of variation in captive bolt gun performance, the efficiency of poll vs frontal shooting and the prevalence of false aneurysms in carotid arteries during shechita and halal slaughter methods. These slaughter methods are religion based and it is mandatory that they be performed by specialised personnel of that religion. Shechita (Jewish) slaughter involves swiftly severing the trachea, carotid arteries and jugular veins using a specialised knife called hallaf, without stunning the animal; while halal slaughter may involve a “religiously acceptable stunning” followed by severing the carotid arteries and jugular veins in a single wipe .
Animal welfare and the quality of meat produced by farmed animals are dependent on all the chain activities to which they are subjected to from birth till slaughter. However, there is lack of clear definition in some areas. There is still need to further investigate this area, interlinking the independent discoveries and information that has been found through studies on some of the contributing factors. Furthermore, the developing world needs to fully investigate, adopt and commit to some of the world’s standard on animal management and meat production thus improving its food security and economy through the use of its maximum potential. It is also important to note that what works for the developed world might not be working in the developing world, hence the need to intensively investigate the matter.
The authors would like to thank the National Research Foundation (NRF): Innovation Doctoral Scholarship (Grant UID: 86113) and Red Meat Research and Development of South Africa (RMRDSA-Authorization number: IT8114/98) for funding this research.
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