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Within all cattle production systems, veal calves are the most severely affected by abomasal damage, with current prevalence at slaughter ranging from 70 to 93% of all animals affected. Although most damage is found in the pyloric region of the abomasum, fundic lesions are also found. Despite past research into the etiology of abomasal damage and the many risk factors that have been proposed, consensus on the causal factors of abomasal damage in veal calves has not yet been reached. The aim of this review was to integrate and analyze available information on the etiology of, and possible risk factors for, abomasal damage in veal calves. We describe various proposed pathways through which risk factors may contribute to damage formation and conclude that the etiology of abomasal damage is most likely multifactorial, with diet being a main contributor. Pyloric lesions, the most common type of damage in veal calves, are likely the result of large and infrequent milk and solid feed meals, whereas fundic lesions may be caused by stress, although the evidence for this is inconclusive. Providing calves with multiple smaller milk and solid feed meals (or ad libitum provision) may decrease abomasal damage. In future research, ulcers, erosions, and scars as well as fundic and pyloric lesions should be recorded separately, because etiologies of these may differ. Further research is required to understand the exact pathway(s) by which milk replacer causes abomasal damage in veal calves; that is, whether low abomasal pH, overloading, or composition are important. Further research is also required to elucidate whether rapid intake of milk replacer and solid feed, which is influenced by restricted amounts fed, inter-calf competition, and calf breed, increases abomasal damage. Research is also needed into the effect of medication and nutrient deficiencies other than iron. The types of experimental designs that can be used for future research could be enhanced if a means to assess abomasal damage antemortem is developed. We conclude that it is unlikely that abomasal or ruminal hairballs, iron deficiency, water provision, and various infections and diseases are significant contributors to abomasal damage in veal calves.
Abomasal damage involves lesions of the inner wall of the ruminant abomasum, which include minor perturbations or more severe damage causing bleeding or perforation of the wall and subsequent peritonitis. Abomasal damage is a problem in cattle of all ages and all production systems, with “white” veal calves (hereafter, veal calves) being most affected (e.g.,
). Abomasal damage in the form of lesions can cause high mortality rates of, for example, between 0.53 and 0.11% in veal calves in Switzerland and Belgium (
). The mortality rates only reflect the most extreme forms of abomasal damage—perforating ulcers—and hence represent only the tip of the iceberg. Average reported prevalence of nonfatal damage at slaughter ranged from 70 to 93% of veal calves in Europe (
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
). Veal calves are reared on a diet made up of milk replacer (MR), supplemented by moderate amounts of solid feed (SF) with a high percentage of concentrate (at least in Europe since 1997), until a slaughter age of approximately 6 mo and a BW of approximately 200 to 250 kg. The MR is typically fed in buckets or troughs twice a day, although some farms use automated milk dispensers, which allow more frequent feedings (typically 3 meals per day;
). The SF is generally only fed after the morning MR meal, in the same container as the MR, once the MR has been consumed. This diet of mostly iron-poor MR and concentrate ensures low blood hemoglobin levels and the pale color of the veal.
The exact implications of abomasal damage for calf welfare are not fully understood. Whether calves experience pain due to nonperforating abomasal damage has not been determined. In most cases, the presence of abomasal damage is not associated with clinical signs (
). Mortality following abomasal perforation, of course, does present a welfare issue. Although it has been proposed that (nonperforating) abomasal damage may reduce feed intake and thus lead to decreased growth and economic losses (
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
Many articles have addressed the causes and predisposing factors of abomasal damage in veal calves and, although no consensus has yet been reached, it is generally accepted that the etiology is multifactorial. The aim of this systematic review is to integrate and analyze the available information on the etiology of, and possible risk factors for, abomasal damage in veal calves. The literature search was conducted from January to April 2017 using the search engine Web of Science, and included the following search terms: Abomas* AND (damage OR ulcer* OR lesion* OR scar*). In addition, the technique of snowballing references (using the reference list of a paper to identify additional papers) was applied. Titles and abstracts were scanned, during which papers referring to non-bovine species or not in English or Dutch were discarded. When no articles on bovines could be identified on a specific mechanism of interest, other ruminant and monogastric articles were used. These other articles were selected based on relevance to the mechanisms of interest only, given that often very few papers were written on the topics we sought, with a preference for ruminant species over monogastric species. Because the fourth stomach compartment of the ruminant, the abomasum, is functionally similar to the monogastric stomach, it may be that knowledge of gastric ulcers extends to abomasal ulcers, although this should be approached cautiously. For some articles, only the abstract could be obtained. This led to 122 articles being evaluated for this review. Despite the fact that veal production systems have changed substantially over the past decades, older literature was included, because experimental studies from that time are often still relevant. This review is divided in 4 parts, covering the association between abomasal damage in veal calves and (1) nutritional factors, (2) stress, (3) diseases, and (4) other miscellaneous factors such as breed and season. We will begin with an overview of lesion type and localization and end by proposing paths for future research.
ANATOMICAL LOCALIZATION AND LESION TYPE
In veal calves, abomasal damage has been commonly described as consisting of 3 types of lesions: erosions, ulcers, and scars (e.g.,
). In this review, we will distinguish between erosions, ulcers, and scars, as these may have slightly different etiologies because of differences in location. Erosions are local defects of the mucosal layer that have not yet penetrated the lamina muscularis mucosae, the thin layer of smooth muscle that separates the lamina propria from the submucosa (
). Ulcers can cause perforation of the abomasal wall, which can lead to inflammation and infection of the peritoneum (peritonitis), the membrane that forms the lining of the abdominal cavity (
). Ulcers have been classified into 4 types. Type 1 ulcers are nonperforating ulcers that come without extensive bleeding; type 2 ulcers are nonperforating and involve (severe) blood loss; type 3 ulcers are perforating with local peritonitis; and type 4 ulcers are perforating with diffuse peritonitis (
). Most experimental studies, however, did not use the latter classification to distinguish between ulcer types. Scars are thought to be healed ulcers, partially because they are found in a similar location and are fibrous contractions of the mucosa (Degen, 1982, as cited by
). No scar tissue is formed in the healing process of erosions because erosions heal using epithelial regeneration, which does not involve the formation of scar tissue (Sun, 1974, as cited by
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
A complete overview of all factors associated with nutrition and their possible role in the development of abomasal damage in veal calves is presented in Table 1.
Table 1Nutritional factors put forward as likely to worsen abomasal damage in veal calves and associated number of studies in support (for) or not in support (against) of these proposed factors
Larger amounts of solid feed worsen damage when amounts are relatively low (500 g/d) or when a large portion is concentrate (80:20). However, when roughage is provided ad libitum, existing damage is not exacerbated.
No, if ad libitum roughage; yes, if mostly concentrate
In the past, European veal calves were fed only MR, until European legislation mandated the provision of fibrous feed in addition to MR in 1997 (European Union Directive 97/2/EC). At slaughter, it was observed that many of the calves fed only MR were suffering from abomasal lesions, with a prevalence of up to 70% (
). An MR-only diet was typically fed in 2 meals per day, and increased linearly in volume throughout the fattening period, ending with provision of approximately 3 kg of MR powder per day (
Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
). The provision of MR has now decreased because of the mandatory provision of SF, the latter being generally provided above the European Union's requirement of 50 to 250 g/d (
). The theory is that an MR-only diet causes abomasal lesions via abomasal overloading or low abomasal pH; however, this has never been studied experimentally and, without further research, it is impossible to know whether these pathways are indeed accurate. Below we present the proposed mechanisms behind these 2 theories and some indirect evidence in support of, or contradicting, these theories. The term “milk” will be used when both MR and whole milk are discussed together or when the distinction is not important. Although overloading and pH are the most mentioned theories in relation to the effect of MR on abomasal damage, the specific milk composition might also affect abomasal damage. No research could be found on the effect of MR composition on abomasal damage; nonetheless, composition will affect the clotting potential of the MR, which might, in some way, affect abomasal damage. This area warrants future attention.
Abomasal Overloading
As explained above, most lesions in veal calves are found near the torus pylorus, which controls the passage of abomasal contents into the duodenum and which is a site of peristalsis and segmentation. Overloading of the abomasum could cause localized hypoxia in the pyloric region (
): the pathway is proposed to start with an increase in the tonus of the abomasal muscles, leading to peristaltic contractions that are strongest around the pylorus. Both these contractions and direct pressure exerted on the abomasal wall by a large milk volume could lead to compression of the mucosa and blood vessels and subsequent oxygen shortage. Over time, damaged sites could develop into erosions and ulcers, although the exact pathway for this is unclear. Current evidence is insufficient to support this theory. The only findings in favor of the overloading theory are 3 articles providing some indirect evidence:
found that group-housed calves that (probably) drank their MR meal faster had more pyloric lesions than individually housed calves that (probably) drank their MR slower; and
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
found that the heaviest calves, hence possibly dominant, faster-drinking calves, developed the most pyloric (but not fundic) lesions. Two articles opposing the overloading theory are
, who found that decreasing milk meal size while simultaneously increasing the concentrate part of the diet caused worse damage (experimental study), and
reported no difference in lumen pH between damaged and intact abomasa of slaughtered bulls, cows, and (nonveal) calves. Pathways explaining the possible relationship between low abomasal pH and abomasal damage are as follows: (1) excessive activation of the proenzyme pepsinogen into pepsin, whereby the proteolytic activity of pepsin may break through the barriers protecting the abomasal wall and cause lesion of mucosal proteins (
); and (2) compromised functioning of the mucus layer that protects the abomasal mucosa, which leads to decreased hydrogen carbonate production and increased back-diffusion of hydrogen ions into the abomasal wall, because fewer ions are neutralized by hydrogen carbonate before coming into contact with the wall (
), the region in which most damage occurs in veal calves.
Indirect evidence that pH may play a role in the development of abomasal damage is the successful treatment of abomasal and gastric ulcers using medication that increases abomasal pH, either by neutralizing secreted HCl or by decreasing HCl secretion, in other mammals (adult cattle:
). Although medication can be used in the treatment of ulcers, lack of knowledge on their long-term (health) consequences limits its application as a preventive measure. Moreover, preventive administration of medication could be considered unethical. It should be noted that the HCl-secretory cells, whose secretions cause abomasal acidity, develop only after a few days of life, possibly to prevent colostral antigens from being broken down (
Abomasal luminal pH in calves depends on meal volume, sucking rate, abomasal emptying rate, acidity of the milk, and the buffering and clotting capacity of the milk (
Abomasal pH and emptying rate in the calf and dairy cow and the effect of commonly administered therapeutic agents. Proc. World Buiatrics Congr., Nice, France.
). The clotting properties of the milk can affect abomasal pH, because whole milk, which has a fast clotting capacity, allows for a lower pH than nonclotting MR (
). Hence, adjusting the milk regimen can affect abomasal pH, and potentially abomasal damage, although no direct evidence has yet been presented for the latter.
Solid Feed
If SF is supplemented to an MR diet, the incidence of abomasal lesions is often observed to worsen (
Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
). However, such an effect has not been found with all roughage types, quantities, and particle sizes. The current theory is that SF can exacerbate damage that has already been caused by large quantities of MR in two ways. The first pathway is by causing trauma, often referred to in the literature as abrasion, to the abomasal wall. The second pathway is by blocking the pylorus, thereby delaying digesta from leaving the abomasum and exacerbating abomasal overloading by extending the time during which large quantities remain in the abomasum (
). The traumatizing capacity of SF is thought to be enhanced by the earlier mentioned increased peristaltic contractions caused by abomasal overloading with MR because those contractions lead to increased contact between the coarse SF and the abomasal wall (
). The effects of SF on abomasal damage may depend on the SF type provided, its physical form, and the amount of SF fed.
Solid Feed Type
Roughage types fed to veal calves include wheat and barley straw, lucerne (or alfalfa), beet pulp, maize silage, and maize cob silage, although the high starch content of maize cob silage makes it similar to concentrate rather than roughage. With the exception of lucerne, these roughage types are chosen because they have a low iron content and thus minimally affect the hemoglobin level of the blood, which helps to preserve the pale color of veal. In research, hay is sometimes fed to veal calves, but this is rarely done on farms, because hay has a high iron content and will cause the meat to darken (
Blokhuis, H. J. 2000. Chain management of veal calf welfare. Final report EU-project contract number FAIR 3 PL96–2049. ID-Lelystad, Lelystad, the Netherlands.
). The effects of roughage on abomasal damage are not entirely clear. Studies have generally found that the feeding of straw, a very coarse roughage, exacerbates abomasal lesions (
Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
) found no significant difference in the pylorus between maize silage and straw but did find more lesions in the fundus of straw-fed calves.
Cereal grains, barley grains, whole-plant maize pellets, and pellet mixes (containing, for example, oat hulls, maize or barley grain, soy flakes or plant oils, and a pellet binder) are the types of concentrate that have been researched in veal calves for their effects on abomasal damage. However, most studies combined both concentrate and roughages in the diet. Only one study added solely concentrate to an MR diet and found a decreasing trend for lesion incidence compared with straw (
). Furthermore, feeding pellets of roughage and concentrate with 4 different compositions (differences were in the starch, fiber, crude protein, and ash contents) did not affect lesions >0.5 cm (
). However, some studies found no improvement or even a worsening of the damage with a combination of roughage and concentrate compared with only roughage (
Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
). It should be noted that no studies used a larger relative proportion of roughage than concentrate, and therefore no general conclusion for all combinations of roughage and concentrate can be made.
The addition of specific feedstuffs, such as extruded pea, extruded soybean, or urea, has been researched to determine their value in adding protein or nitrogen to the diet without compromising veal color and quality. No effect on the incidence or severity of abomasal lesions was found with the addition of these feedstuffs (
Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
A feedstuff can be provided in various physical forms. Roughage can be fed as large particles, chopped to a smaller particle size, ground, or included in a pellet. Different physical forms may have different traumatizing or blocking effects, and one might expect that larger particles are more blocking than shorter ones and therefore cause more abomasal lesions. Shorter particles, however, may be sharper and may become stuck in the abomasal wall more easily. Chopping wheat straw to particle sizes equal to those of barley grain lowered lesion incidence to approximately equal levels for the 2 feedstuffs, supporting the theory that longer particles cause more damage, although the severity of the lesions was higher for barley grain (
Growth performance, behaviour, forestomach development and meat quality of veal calves provided with barley grain or ground wheat straw for welfare purpose.
found no effect of providing roughages in long-chopped, short-chopped, or ground form.
For pelleted feeds, it would be expected that their finer particles would have a lesser traumatizing or blocking effect on the abomasal mucosa or pyloric sphincter, respectively, and thereby cause less damage to the abomasum. However, no difference in abomasal damage was found between straw and straw pellets (
), which contradicts this hypothesis. In addition, pelleted maize silage was observed to cause more lesions than short-chopped or ground maize (cob) silage (
). Whether this difference is actually due to the pelleted form or to the different roughage types cannot be determined from these studies. Nevertheless, the lack of difference between straw and pelleted straw implies that roughage type is the main determinant here.
Amount of Solid Feed
In addition to type and physical form of roughage, the amount of SF fed may affect abomasal damage. Larger amounts are expected to increase trauma to the abomasal wall and worsen blocking of the pyloric sphincter, thereby increasing abomasal damage. Indeed, larger, but still restricted, amounts of roughage have been shown to increase the prevalence and size of ulcers (
), which may be linked to the inclusion of concentrate in the diet, as theorized before. In contrast, inclusion of a high level of concentrate (concentrate:roughage 80:20) does increase abomasal damage when the amount fed increases (
). For some roughage sources, an interaction between the amount fed and the type of roughage was found, where the source was only severely damaging when fed in larger amounts. For example, maize (cob) silage caused fewer lesions than straw at small amounts (250 g/d) and more lesions than straw in larger amounts (500 g/d;
). A finding that contradicts the hypothesis that larger amounts of SF lead to more abomasal damage is that provision of straw or hay ad libitum does not exacerbate lesions caused by MR (
). We may speculate that ad libitum provision allows the individual calf to select a diet that is quantitatively optimal for its body, including its abomasum. Furthermore, it minimizes competition between pen mates and allows meals throughout the day, likely reducing feeding rate and meal size. Alternatively, rumen development may play a role (see the Rumen Development section). Finally,
Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
proposed that the moment at which the SF is consumed might matter. Consumption of SF immediately after the abomasum has been filled with a large quantity of MR may exacerbate overloading and increase abomasal damage.
Rumen Development
Before entering the abomasum, SF must pass the 3 other stomach compartments. In the first, the rumen, SF will be fermented. It has been hypothesized that feed will be less coarse when it enters the abomasum if this feed is well fermented (
). In addition, because of the smaller particle size resulting from good or better fermentation, SF should also block the pylorus less frequently than when fermented incompletely. Because calves are born with a nonfunctional rumen, its development affects the extent to which SF is fermented. Beef calves and lambs are more susceptible to abomasal perforation caused by ulcers during the development from preruminant to ruminant, which normally occurs at approximately 4 to 8 wk of age (
). This can be achieved using a feeding regimen aimed at early rumen development (ERD), which includes feeding both roughage and concentrate from an early age onward. An increase in rumen volume and weight is stimulated by the feeding of fibrous feeds, whereas the development of rumen papillae is stimulated by volatile fatty acids and therefore by less fibrous feeds (
In support of this theory, one study found that calves with better developed rumens had fewer abomasal lesions than calves with less developed rumens (
). However, when the ERD theory was tested by adjusting calf diet before the age of 12 wk, it was found that ERD only decreases the incidence of scars (
). These findings suggest that ERD protects calves from developing abomasal ulcers during the early weeks of life, leading to less scarring later on, but that it has no effect on ulcer or erosion development in later life. Two years later, the same authors confirmed that better rumen development does not protect against abomasal damage at a later age (
), based on the finding that both rumen development score and abomasal damage increased for increasing SF amounts (when the proportion of concentrate was high).
Hairballs
Hairballs (or trichobezoars) are round masses composed of ingested hair (
proposed that ruminal hairballs might prevent proper digestion in the rumen, which would allow large feed particles to pass through the first 3 stomach compartments into the abomasum. These underfermented particles may cause trauma to the abomasal mucosa or block the pyloric exit. Rumen motility, which can be improved by feeding SF in addition to MR, aids in the removal of hair from the rumen, thereby preventing the development of hairballs (
), during which hair can be ingested. Calves fed straw or hay have less hair in their rumen than calves fed maize (cob) silage, with those fed maize silage being intermediate, and the amount of hair was further reduced as roughage particle size was increased (
Comparing the effects of different roughage diets on grooming behaviour and hairball prevalence in veal calves.
in: Lidfors L. Blokhuis H. Keeling L. Proc. 44th Congr. Int. Soc. Appl. Ethol. (ISAE), Uppsala, Sweden. Wageningen Academic Publishers,
Wageningen, the Netherlands2010: 16
found that calves fed only milk had more ruminal hairballs and fewer abomasal lesions than calves fed additional roughage (with the exception of ad libitum hay, for which ulcer incidence was not increased). This implies that ruminal hairballs are at least not a prerequisite for the development of abomasal lesions.
Hairballs can also be found inside the abomasum, although this is only true in veal calves fed only MR. Abomasal hairballs have been hypothesized to cause trauma to the abomasal mucosa or to block the pylorus, both of which may lead to abomasal damage (
). Only one study on veal calves measured the presence of both hairballs and lesions in the abomasum, but a relationship between the two was not evaluated (
). Despite these inconclusive results, veterinarians and researchers tend to assume a relationship between hairball presence in the abomasum and abomasal lesions (
), only one study on veal calves researched part of this relationship. That study found no effect of iron supplementation on abomasal damage, in calves fed MR only (
). When beef calves were supplied with a free-choice mineral mix, a nonsignificant trend for a decreased need for abomasal surgery due to ulceration was observed (
). This implies a role for nutrient deficiencies in abomasal ulceration (composition of the mineral mix is unknown but can be assumed to differ between the farms the calves originated from). In another study, deficiencies in copper or selenium occurred more often in beef calves with (perforating) abomasal damage (
It has been theorized that a low serum copper concentration can lead to a derangement of elastin cross-linkages in the abomasal wall, compromising the abomasal mucosa and microvasculature and leaving the abomasal wall prone to damage (
). In addition, copper deficiency can lead to decreased neutrophil function and subsequently to an increased risk of infection, as occurs when the abomasum is damaged (
). Because a high concentration of zinc, molybdenum, or sulfur reduces the availability of copper, surplus of these minerals can exacerbate the problem of copper shortage. Thus, in beef calves, nutrient deficiencies, at least for copper and selenium, appear to affect abomasal damage. Whether the same occurs in veal calves has not yet been studied.
Water
Veal calves receive fluids from milk, from other feeds provided, from the drinking of free water, and from the oxidation of food and body tissue. Whereas water originating from feed and free water is deposited in the rumen, water originating from milk generally bypasses the rumen and is deposited in the abomasum (
). However, consumption of water was, in that study, strongly linked to the provision of SF and ruminal plaque, indicating that SF may have caused the damage in that case.
THE FACTOR OF STRESS
In many monogastric species, acute stress has been experimentally shown to cause ulceration of the stomach mucosa (rat:
). In ruminants, such as calves, the abomasum acts similarly to the monogastric stomach. In some cases, the stress-induced lesions of monogastrics resemble the ulcers found in the calf fundus (
). Proposed pathways through which stress could cause abomasal damage have a common starting point, whose involvement has been demonstrated only in rats. In rats, ulcers caused by stress only develop after a drop in body temperature (
), which initiates 2 main pathways: (1) increased production of gastric acids, whose effects were described previously (see section titled Low Abomasal pH); and (2) a decrease in the rhythm of stomach contractions from 6 to 7 to only 0.5 to 2 times per minute, which leads to decreased mucosal blood flow and subsequent damage through local hypoxia, mechanical damage, and decreased function of the mucosa-protecting mucus and cytoprotective prostaglandins (
It has been proposed that abomasal ulcers in veal calves are not related to stress, because the location of these ulcers is not similar to that of ulcers caused by stress in adult cattle (
). In veal calves, ulcers are predominantly found in the pyloric region, whereas in adult cattle they are predominantly found in the fundic region. It is unclear what this assumption of stress being a causal factor in adult cattle is based on.
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
found that calves in conventional veal systems had more fundic but not pyloric lesions than animals kept in a potentially less stressful system in which they had more square meters per individual, could go outdoors and received water and roughage ad libitum.
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
proposed, therefore, that stress might be involved in the development of fundic but not pyloric lesions. In that study, however, diet was also an important difference between these 2 rearing systems. Other studies did not identify links between stress and abomasal damage in veal calves, regardless of the treatments that were used: individual housing versus group housing (
). Furthermore, calves used to human–calf interactions (gentled calves), which involved the stockperson talking to and stroking the calves and letting the calf suck the person's fingers for 90 s following feeding, had fewer pyloric lesions at slaughter (
). Because the human–calf interaction allowed calves to suck on the stockperson's fingers, enhanced saliva production might also have decreased abomasal acidity and consequently ulceration. In that case, the difference found would be unrelated to stress, as also suggested by the absence of differences in stress measurements (behavioral observations, response to ACTH challenge) between gentled and control calves.
Calves performing more of the abnormal oral behavior tongue rolling or playing were found to have significantly fewer abomasal ulcers and scars but not fewer erosions (
). In addition, in a more recent study, the same relationship was found between abomasal lesions and tongue playing as well as oral manipulation of the environment (
). Stereotypies, such as these abnormal oral behaviors, are defined as repetitive and invariant behavioral patterns that lack an obvious goal or function (
). Calves that tongue roll may develop less abomasal damage due to reduced stress through better coping. Similarly, rats that were exposed to acute stress, in the form of electric shocks, developed more gastric ulcers when punished for attempting to escape these shocks, which denies the rats a way to cope with the acute stress (
). Other mechanisms might be that extra saliva produced when performing abnormal oral behaviors would increase abomasal pH, although it could be argued that saliva produced during object manipulation may not enter the gastrointestinal tract, or that increased satisfaction of oral eating behaviors decreased milk intake and thereby abomasal overloading.
FACTORS ASSOCIATED WITH DISEASE
Microorganisms
Infections caused by fungi, bacteria, parasites, and diseases caused by viruses are hypothesized to lead to the development of abomasal damage in calves (
); see Table 2, Table 3, 4, and 5 for an overview of these studies. This hypothesis is partly because microorganisms are known to cause peptic ulcers in humans (
). In calves, fungi have been isolated from abomasal lesions but evidence for a causal role is currently insufficient (Table 2). Studies investigating bacterial involvement are more abundant; however, bacteria isolated from lesions may originate from postmortem colonization. Additionally, administration of bacteria leads to a different type of damage than is commonly observed in veal calves; namely, numerous small ulcers spread throughout the abomasum (Table 3). Furthermore, although some parasites are capable of causing ulcers in calves (
), it is unlikely and not reported that indoor-housed calves, fed on concentrate and silages, are exposed to these parasites. Moreover, the type of abomasal damage caused by parasites, referred to as nodules, is quite different from that described most commonly in veal calves (Table 4). Finally, although some viruses can cause lesions in several organs (including the abomasum) in dairy calves (
). Viruses, although possibly causing some of the cases of abomasal damage found in veal calves (Table 5), are unlikely to be a main factor in the majority of damage found. However, given the small amount of research in this area, we encourage further focus on this area. Noninfectious diseases, left abomasal displacement, and certain types of tumors might also cause abomasal ulcers in adult cattle and, in very rare cases, calves (
The relationship between the presence of Helicobacter pylori, Clostridium perfringens type A, Campylobacter spp., or fungi and fatal abomasal ulcers in unweaned beef calves.
Experimental induction of abdominal tympany, abomasitis, and abomasal ulceration by intraruminal inoculation of Clostridium perfringens type A in neonatal calves.
Veal calves in Europe (Belgium and the Netherlands) have been reported to be the group of farm animals receiving the most antimicrobial (AM) treatments (
Bondt, N., L. Puister, L. Ge, H. van der Veen, R. Bergevoet, B. Bouma, A. van Vliet, and K. Wehling. 2012. MARAN—Trends in veterinary antibiotic use in the Netherlands 2004–2012. LEI, Wageningen UR, Wageningen, Netherlands.
), likely as a direct consequence of the mixing of young, low-immunity calves from many different origins. In Belgium, over 40% of calves were treated with AM every day of the production cycle (
). Although much less frequently used than AM drugs, (non)steroidal anti-inflammatory drugs [(N)SAID] are also given to veal calves; of all treatments in Belgian veal calves in 2009, 88% was AM and 12% was NSAID (
). Medication is widely used in veal calves and could be an important factor in the development of abomasal damage; however, the current evidence for this is nonexistent and future research is warranted. Nonetheless, the use of NSAID lies far below the prevalence of abomasal damage in veal calves and is unlikely to be one of the main factors.
OTHER FACTORS
Breed
It has been proposed by some authors that the breed of calf may affect abomasal damage. For example, Montbéliarde calves develop more pyloric scars than Holstein Friesian calves when kept in similar systems (
). However, it should be noted that Montbéliarde calves are also capable of growing faster, which is accompanied by a higher MR and SF intake, and thus possibly more severe overloading of the abomasum. This was confirmed by both
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
, who found no effect of breed on pyloric lesions although, in these studies, breeds were categorized in 3 groups (dairy breeds, cross-breeds, and other breeds) and only those groups were compared, not individual breeds. Breed might have an important impact on abomasal lesions when a particular breed is able to consume more MR and SF more rapidly.
Seasonal Effects
In adult cattle and in beef cattle, occurrence of abomasal damage differs between seasons. In adult dairy cattle, this could be related to the seasonality of milk production, because most ulcers develop around parturition, a period marked by stress and a severe change in diet (
). It is theorized that calves do not nurse when the weather is bad, which leads to a drop in abomasal pH, leaving the abomasum vulnerable to ulceration. When the weather is better, calves overconsume milk, which leads to abomasal overloading. In one study, the seasonal effect was fully explained by the use of a seasonal beef production system, indicating that other season-related effects, such as pasture growth, were not causal (
Because veal calves originate mostly from a nonseasonal dairy system, are kept inside, and do not nurse their dams, bad weather should not have an effect on abomasal damage. Nevertheless, a risk assessment conducted by
showed that veal calves have a higher risk of developing pyloric lesions when they are raised in the summer or autumn and the lowest risk when reared in spring, both compared with winter. Why this effect exists is unknown. We may speculate that it correlates with other (as yet unidentified) factors that differ seasonally or that differences in living conditions between seasons on the dairy farm of origin have a predisposing effect. Temperature fluctuations in the stable, which can occur if temperature is not regulated year round, might have an effect; for example, through cold or heat stress. As mentioned before, fluctuations in body temperature of rats can lead to the development of stomach ulcers (
). Alternatively, calves may be fed more or ingest feed faster in certain seasons.
Housing and Management
Certain aspects of housing and management have also been associated with lesion prevalence via surveys. Absence of a heating system and regular visits of a veterinarian appear to be linked to the occurrence of pyloric lesions (
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
). It is unlikely that these factors have a direct effect on abomasal lesions; instead, they likely correlate with other factors that do have a direct effect, such as stress or fluctuations in temperature.
Individual Susceptibility
Finally, it has been proposed that calves differ in individual susceptibility to abomasal lesions, because calves kept in similar systems, either on the same or on another farm, can show very different degrees of abomasal lesion. This is also observed within pens (
). Where some calves show severe ulceration, other calves kept under the same conditions may have completely undamaged abomasa. Thus, calves are not equally susceptible to abomasal ulceration (
), possibly because of the different mechanisms with which calves cope with stress (and stress is likely associated with fundic lesions). In addition, faster-growing calves are more susceptible to damage (
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
). This implies that the difference is not due to individual susceptibility but perhaps to more abomasal overloading in faster-growing calves. It has been suggested that only by offering calves free choice of diet can an appropriate diet be provided for each individual calf (
). Whether this is the case in calves has, to our knowledge, never been studied. Nevertheless, if abomasal damage in calves indeed has a heritable component, the application of this finding is likely limited, because veal calves originate from the dairy sector, in which other breeding factors are important.
SUMMARY AND CONCLUSIONS
The aim of this review was to integrate the information currently available on the etiology of, and risk factors for, abomasal damage in the form of ulcers, erosions, and scars. Some information may have been excluded because it was in a (for us) foreign language (articles included were in Dutch or English). In addition, extrapolation of results from the older literature may not be fully accurate, because the growing systems in which veal calves are kept have changed substantially over time. Nevertheless, experimental studies from earlier periods can still provide useful information. An overview of all proposed factors and associated literature support or evidence is presented in Table 6. An overview of the most likely factors and the associated mechanisms is presented in Figure 1. Although a clear effect on the development of abomasal damage was not identified for all proposed factors, it is clear that the etiology is multifactorial, with various dietary factors contributing to pyloric lesion formation extensively and fundic lesions probably being linked to stress. Pyloric lesion incidence can likely be reduced by feeding smaller quantities of milk replacer in more frequent meals that, from an early age, should be combined with SF in the form of both concentrate and roughages. In addition, decreasing the level of stress experienced by veal calves may decrease the occurrence of fundic lesions and improve overall animal welfare by minimizing negative experiences.
Table 6Overview of current knowledge on all proposed risk factors of abomasal damage in veal calves, with associated number of studies in support (for) or not in support (against) of these proposed factors
Only studies specifically studying veal calves are included here.
Factor
For
Against
Summary of findings
Important
Milk replacer (MR)
4
2
Despite little actual experimental study in this field, MR is likely to play an important role. The exact pathways are unknown.
Yes
Solid feed
9
2
Solid feed provision on top of MR is likely to affect the level of damage, unless roughage is provided ad libitum.
Yes
Rumen development
3
1
The evidence for rumen development protecting against abomasal damage is limited, but studies showing that ad libitum provision of roughage does not exacerbate damage support this hypothesis.
Probably
Hairballs
0
1
Both hairballs in the rumen and abomasum do not show a clear association with abomasal lesions.
Substantial confounding factor of nutrition (Bähler et al., 2010).
4
Despite studies showing a link between stereotypies and lower damage (not included here), the link with stress is not strong in veal calves, except for fundic lesions, which are not the most common in this group of animals.
Two of these studies found damage very different from that commonly found in veal calf abomasa.
3
Studies that found a link between bacteria and abomasal damage found very different patterns of damage; that is, many small lesions widespread across the abomasum.
Unlikely
Viruses
0
0
No research in veal calves. The prevalence of viruses that cause abomasal damage is much lower than the prevalence of abomasal damage, making a viral factor unlikely to be a main contributor to lesions veal calves.
Unlikely
Fungi
0
0
No research in veal calves.
Unknown
Parasites
0
0
No research in veal calves. In dairy calves, damage caused by parasites are nodules, which are very different from damage commonly observed in veal calves.
No
Breed
1
2
Breed is probably only relevant when it affects growth rate: hence feeding speed and amounts ingested.
Unknown
Medication
0
1
Too little medication specifically tested. Medication is widespread enough to be linked to damage.
Unknown
Season
1
0
Too little work on this. Probably only has an indirect effect.
Unknown
Housing
2
0
Too little work on this. Probably only has an indirect effect.
Unknown
Growth rate
1
0
Although there is little work on this, our own unpublished work suggests that calves that grow faster have more damage.
Yes
Genetics
0
0
No study.
Unknown
1 Only studies specifically studying veal calves are included here.
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
Figure 1Schematic overview of the most likely risk factors for abomasal damage and the pathways through which these operate. Early rumen development can mitigate trauma, at least during early life.
In future research, pyloric and fundic lesions, as well as lesion types (i.e., ulcer types 1–4, erosions, or scars), should be scored separately. More research is required to understand the precise pathways by which MR causes such a high prevalence of abomasal lesions in veal calves. Further research is also warranted on the effect of rapid intake of MR and SF caused by restricted amounts, competition, and breed. More research is needed on the impact of medication, the chemical composition of the MR, and into deficiencies of other nutrients than iron, especially copper and selenium. Finally, no studies have yet focused on the effects of the abomasal emptying rate on abomasal damage; in adult cattle, delayed abomasal emptying has been proposed as a risk (
Abomasal pH and emptying rate in the calf and dairy cow and the effect of commonly administered therapeutic agents. Proc. World Buiatrics Congr., Nice, France.
). Another important path of research would be to develop a method that can assess abomasal damage antemortem. Currently, calves must be killed to assess and measure the extent of abomasal damage, which limits the experimental design options. The finding that calves that grow fastest develop most abomasal lesions (
Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
) could be used for this purpose. Finally, the link between abomasal damage and animal welfare, or more specifically pain, is not well understood and has received no research attention to our knowledge. Whether these lesions are painful, and if so, which types are painful and how severe the pain is, is of crucial importance because this health problem is widespread in the veal industry. One complication here is that commonly used indicators of pain in calves, such as growth rate and feeding rate, are linked to the etiology of the problem at hand. Other indicators of pain (e.g., facial expressions) will have to be investigated.
ACKNOWLEDGMENTS
This paper is the result of a stimulating discussion at the 50th Congress of the International Society for Applied Ethology, held in Edinburgh in 2016. We thank all the lovely people involved in this discussion on abomasal damage in calves: Margit Bak Jensen (Aarhus University, Denmark), Anne Marie de Passillé and Jeff Rushen (University of British Columbia, Canada), Eddie Bokkers and Kees van Reenen (Wageningen University and Research, the Netherlands), Laura Hänninen (University of Helsinki, Finland), and Derek Haley (University of Guelph, Canada).
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