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Invited review: Abomasal damage in veal calves

Open ArchivePublished:December 24, 2018DOI:https://doi.org/10.3168/jds.2018-15292

      ABSTRACT

      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.

      Key words

      INTRODUCTION

      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.,
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ;
      • Kureljušić B.
      • Ivetić V.
      • Savić B.
      • Jezdimirović N.
      • Cvetojević D.
      • Kureljušić J.
      • Ilić Ž.
      • Stanojević S.
      • Stevančević M.
      Pathomorphological characteristics of abomasal ulcers in high-yielding dairy cows.
      ;
      • Hund A.
      • Beer T.
      • Wittek T.
      Abomasal ulcers in slaughtered cattle in Austria.
      ). 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 (
      • Bähler C.
      • Steiner A.
      • Luginbühl A.
      • Ewy A.
      • Posthaus H.
      • Strabel D.
      • Kaufmann T.
      • Regula G.
      Risk factors for death and unwanted early slaughter in Swiss veal calves kept at a specific animal welfare standard.
      ;
      • Pardon B.
      • De Bleecker K.
      • Hostens M.
      • Callens J.
      • Dewuif J.
      • Deprez P.
      Longitudinal study on morbidity and mortality in white veal calves in 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 (
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
      ;
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ). Certain veal farms in Europe have reported 100% prevalence for abomasal damage (
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ). 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;
      • Bokkers E.A.M.
      • Koene P.
      Activity, oral behaviour and slaughter data as welfare indicators in veal calves: A comparison of three housing systems.
      ;
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ). 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 (
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Hund A.
      • Beer T.
      • Wittek T.
      Abomasal ulcers in slaughtered cattle in Austria.
      ), unless the lesions are severe enough to perforate the abomasal wall or cause hemorrhage (
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ,
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Predictive values for clinical signs of abomasal ulcer disease in adult dairy cattle.
      ). Commonly, affected veal calves are found dead in the stable or lesions are only identified at slaughter (
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ). 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 (
      • Tajik J.
      • Nazifi S.
      • Heidari M.
      • Babazadeh M.
      Evaluation of serum proteins in water buffaloes (Bubalus bubalis) with abomasal ulcer.
      ), most studies have been unable to identify a reduction in growth (
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Van Dijk S.
      • Mevius D.
      Effect of clenbuterol on the incidence of abomasal lesions in veal calves.
      ;
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      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.,
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ;
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ), although other methods, such as estimated surface area, have recently been applied to record lesion severity (
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      ). 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 (
      • Mattiello S.
      • Canali E.
      • Ferrante V.
      • Caniatti M.
      • Gottardo F.
      • Cozzi G.
      • Andrighetto I.
      • Verga M.
      The provision of solid feeds to veal calves: II. Behavior, physiology, and abomasal damage.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). They are small compared with ulcers, usually only 1 to 20 mm in diameter (Sun, 1974;
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ), with more recent studies reporting mean erosion sizes of 0.7 cm2 (
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). In addition, erosions are likely to have a lower prevalence than ulcers (
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). Ulcers are lesions of the abomasal mucosa that penetrate into the submucosa and range from a few millimeters to several centimeters in size (
      • Mattiello S.
      • Canali E.
      • Ferrante V.
      • Caniatti M.
      • Gottardo F.
      • Cozzi G.
      • Andrighetto I.
      • Verga M.
      The provision of solid feeds to veal calves: II. Behavior, physiology, and abomasal damage.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). 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 (
      • Jensen R.
      • Pierson R.E.
      • Braddy P.M.
      • Saari D.A.
      • Benitez A.
      • Lauerman L.H.
      • Horton D.P.
      • McChesney A.E.
      Fetal abomasal ulcers in yearling feedlot cattle.
      ;
      • Tanwar R.K.
      • Chahar A.
      • Fakhruddin
      • Singh A.P.
      • Bihani D.K.
      Abomasal ulcers in cattle.
      ). 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 (
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Van Immerseel F.
      • Pardon B.
      • Maes S.
      • Heyndrickx M.
      • Timbermont L.
      • Boyen F.
      • Haesebrouck F.
      • Ducatelle R.
      • Deprez P.
      Isolation of a clonal population of Clostridium perfringens type A from a Belgian Blue calf with abomasal ulceration.
      ). 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
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). When abomasal ulcers heal, the wound contracts and new scar tissue is synthesized (
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ). 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
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ). In veal calves, abomasal damage is mostly found in the pyloric region of the abomasum (
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ;
      • De Wilt J.G.G.
      Behaviour and welfare of veal calves in relation to husbandry systems. PhD Thesis.
      ;
      • Welchman D.D.
      Associations between feeding, housing and the incidence of abomasal ulcers in veal calves.
      ;
      • Pearson G.R.R.
      • Welchman D.
      • Wells M.
      Mucosal changes associated with abomasal ulceration in veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Van Dijk S.
      • Mevius D.
      Effect of clenbuterol on the incidence of abomasal lesions in veal calves.
      ;
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ). Nevertheless, erosions can also be found scattered throughout the abomasum (
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ) and in the fundic region, though with lower prevalence and severity (Groth and Berner, 1971 as cited by
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ;
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
      ;
      • Valgaeren B.R.
      • Pardon B.
      • Flahou B.
      • Verherstraeten S.
      • Goossens E.
      • Timbermont L.
      • Haesebrouck F.
      • Ducatelle R.
      • Van Immerseel F.
      • Deprez P.R.
      Prevalence and bacterial colonisation of fundic ulcerations in veal calves.
      ).

      FACTORS ASSOCIATED WITH NUTRITION

      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
      FactorForAgainstSummary of findingsConclusion
      The bold typeface indicates those factors that might contribute most to abomasal damage.
      Milk replacer (MR)
       Abomasal overloading42No direct evidence, except that potentially faster drinking calves have worse damage.Unknown
       Low abomasal pH00No study has assessed this link.Unknown
      Solid feed
       Roughages vs. MR only92Roughages tend to exacerbate existing damage caused by MR, except when provided ad libitum.Yes, in restricted amounts
       Coarse vs. less coarse roughages65In restricted amounts, straw tends to worsen damage compared with only MR or other types of roughage.Yes, in restricted amounts
       Roughages vs. concentrate23Concentrates cause less damage when small amounts are provided. In large amounts, concentrates are worse than roughage.Yes, in small amounts
       Larger particles of roughage1
      Larger particles = more but less severe lesions.
      4This is not supported by experimental evidence.No
       Increasing amounts of solid feed23Larger 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
       Poor rumen development31
      Large quantities of concentrate led to better rumen development but worse damage.
      Rumen development may protect against abomasal damage when large quantities of concentrate are not provided.Probably
       Ruminal hairballs01This is not supported by experimental evidence.No
       Abomasal hairballs00No study has assessed this link in veal calves.Unknown
      Nutrient deficiency
       Iron deficiency01This is not supported by experimental evidence.No
       Copper deficiency00No study has assessed this link in veal calves.Unknown
      Water
       Water provision11Evidence is inconclusive, but the only experimental study is against.Unlikely
      1 The bold typeface indicates those factors that might contribute most to abomasal damage.
      2 Larger particles = more but less severe lesions.
      3 Large quantities of concentrate led to better rumen development but worse damage.

      Milk Replacer

      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% (
      • Wensing T.
      • Breukink H.J.
      • Van Dijk S.
      The effect of feeding pellets of different types of roughage on the incidence of lesions in the abomasum of veal calves.
      ;
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ). 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 (
      • Prevedello P.
      • Brscic M.
      • Schiavon E.
      • Cozzi G.
      • Gottardo F.
      Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). 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 (
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ). 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 (
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ;
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ): 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:
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      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
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
      and
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      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
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      , who found that decreasing milk meal size while simultaneously increasing the concentrate part of the diet caused worse damage (experimental study), and
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      , who found that calves receiving relatively low amounts of MR had a higher risk for lesions (risk assessment study).

      Low Abomasal pH

      In rats, horses, and humans, a low gastric pH has been associated with a higher frequency of gastric ulceration or eroding (
      • Nagamachi Y.
      • Skoryna S.C.
      Relationship between gastric mucosal pH and site of peptic ulceration.
      ;
      • Murray M.J.
      Review article: Pathophysiology of peptic disorders in foals and horses: A review.
      ;
      • Uchida M.
      • Takayama M.
      • Kato Y.
      • Tsuchiya S.
      • Horie S.
      • Watanabe K.
      A novel method to produce extensive gastric antral ulcer in rats: Pharmacological factors involved in the etiology of antral ulceration.
      ). In adult beef cattle, a lower pH has been associated with more abomasal erosion (
      • Jensen R.
      • Spraker T.R.
      • Glock R.D.
      • Jones R.L.
      • Collins J.K.
      • Flack D.E.
      • Kerschen R.
      • Hoff R.L.
      Abomasal erosions in feedlot cattle.
      ), which has led to the proposition that pH may also be an important factor in abomasal damage in calves (
      • Ahmed A.F.
      • Constable P.D.
      • Misk N.A.
      Effect of feeding frequency and route of administration on abomasal luminal pH in dairy calves fed milk replacer.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ). There is no direct evidence currently for this, however. In fact,
      • Hund A.
      • Beer T.
      • Wittek T.
      Abomasal ulcers in slaughtered cattle in Austria.
      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 (
      • Nagamachi Y.
      • Skoryna S.C.
      Relationship between gastric mucosal pH and site of peptic ulceration.
      ;
      • Ahmed A.F.
      • Constable P.D.
      • Misk N.A.
      Effect of feeding frequency and route of administration on abomasal luminal pH in dairy calves fed milk replacer.
      ;
      • Mesarič M.
      • Zadnik T.
      • Klinkon M.
      Comparison of serum pepsinogen activity between enzootic bovine leukosis (EBL) positive beef cattle and cows with abomasal ulcers.
      ); 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 (
      • Nagamachi Y.
      • Skoryna S.C.
      Relationship between gastric mucosal pH and site of peptic ulceration.
      ;
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ;
      • Yandrapu H.
      • Sarosiek J.
      Protective factors of the gastric and duodenal mucosa: An overview.
      ). In support of the latter, mucin concentration was reported to be lower at damaged sites (
      • Pearson G.R.R.
      • Welchman D.
      • Wells M.
      Mucosal changes associated with abomasal ulceration in veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ) and in the pyloric region (
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ), 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:
      • Tharwat M.
      • Ahmed A.F.
      Abomasal ulceration in buffaloes and cattle: Clinico-biochemical and pathological findings.
      ; sheep:
      • Morgado A.A.
      • Nunes G.R.
      • Martins A.S.
      • Hagen S.C.F.
      • Rodrigues P.H.M.
      • Sucupira M.C.A.
      Metabolic profile and ruminal and abomasal pH in sheep subjected to intravenous ranitidine.
      ; musk-ox, moose, deer, and wapiti:
      • Haigh J.C.
      Cimetidine for the treatment of abomasal ulcers in young ruminants.
      ; humans:
      • Maton P.N.
      • Burton M.E.
      Antacids revisited.
      ;
      • Holle G.E.
      Pathophysioogy and modern treatment of ulcer disease.
      ). 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 (
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ;
      • Weiner H.
      Use of animal models in peptic ulcer disease.
      ;
      • Guilloteau P.
      • Zabielski R.
      • Blum J.W.
      Gastrointestinal tract and digestion in the young ruminant: Ontogenesis, adaptations, consequences and manipulations.
      ).
      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 (
      • Woodford S.T.
      • Whetstone H.D.
      • Murphy M.R.
      • Davis C.L.
      Abomasal pH, nutrient digestibility, and growth of Holstein bull calves fed acidified milk replacer.
      ;
      • Ahmed A.F.
      • Constable P.D.
      • Misk N.A.
      Effect of feeding frequency and route of administration on abomasal luminal pH in dairy calves fed milk replacer.
      ;
      • Constable P.D.
      • Ahmed A.F.
      • Misk N.A.
      Effect of suckling cow's milk or milk replacer on abomasal luminal pH in dairy calves.
      ,
      • Constable P.D.
      • Wittek T.
      • Ahmed A.F.
      • Marshall T.S.
      • Sen I.
      • Nouri M.
      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.
      ). Smaller milk volumes provided multiple times a day maintain a higher and more stable abomasal pH than infrequent large meals (
      • Woodford S.T.
      • Whetstone H.D.
      • Murphy M.R.
      • Davis C.L.
      Abomasal pH, nutrient digestibility, and growth of Holstein bull calves fed acidified milk replacer.
      ;
      • Ahmed A.F.
      • Constable P.D.
      • Misk N.A.
      Effect of feeding frequency and route of administration on abomasal luminal pH in dairy calves fed milk replacer.
      ). Normally, acidified MR would lead to a decreased abomasal pH compared with normal MR (
      • Vajda V.
      • Maskaľová I.
      • Tesfaye A.
      Acid-base homeostasis of blood and pH of abomasum in calves fed non-acidified and acidified milk replacer.
      ); however, acidified MR can be provided ad libitum, leading to more frequent consumption (
      • Webb L.E.
      • Engel B.
      • Berends H.
      • Van Reenen C.G.
      • Gerrits W.J.J.
      • De Boer I.J.M.
      • Bokkers E.A.M.
      What do calves choose to eat and how do preferences affect behaviour?.
      ), although not all studies support this (
      • Hill T.M.
      • Bateman H.G.
      • Aldrich J.M.
      • Quigley J.D.
      • Schlotterbeck R.L.
      Evaluation of ad libitum acidified milk replacer programs for dairy calves.
      ). 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 (
      • Constable P.D.
      • Ahmed A.F.
      • Misk N.A.
      Effect of suckling cow's milk or milk replacer on abomasal luminal pH in dairy calves.
      ). 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 (
      • Wensing T.
      • Breukink H.J.
      • Van Dijk S.
      The effect of feeding pellets of different types of roughage on the incidence of lesions in the abomasum of veal calves.
      ;
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ;
      • Veissier I.
      • Boissy A.
      • DePassillé A.M.
      • Rushen J.
      • Van Reenen C.
      • Roussel S.
      • Andanson S.
      • Pradel P.
      Calves' responses to repeated social regrouping and relocation.
      ;
      • Mattiello S.
      • Canali E.
      • Ferrante V.
      • Caniatti M.
      • Gottardo F.
      • Cozzi G.
      • Andrighetto I.
      • Verga M.
      The provision of solid feeds to veal calves: II. Behavior, physiology, and abomasal damage.
      ;
      • Cozzi G.
      • Brscic M.
      • Gottardo F.
      Main critical factors affecting the welfare of beef cattle and veal calves raised under intensive rearing systems in Italy: A review.
      ;
      • Berends H.
      • Van Reenen C.G.
      • Stockhofe-Zurwieden N.
      • Gerrits W.J.J.
      Effects of early rumen development and solid feed composition on growth performance and abomasal health in veal calves.
      ;
      • Prevedello P.
      • Brscic M.
      • Schiavon E.
      • Cozzi G.
      • Gottardo F.
      Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). 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 (
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ;
      • Mattiello S.
      • Canali E.
      • Ferrante V.
      • Caniatti M.
      • Gottardo F.
      • Cozzi G.
      • Andrighetto I.
      • Verga M.
      The provision of solid feeds to veal calves: II. Behavior, physiology, and abomasal damage.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). 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 (
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ). 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 (
      • Van der Mei J.
      The incidence of abomasal lesions in veal calves fattened in two housing systems and fed with or without straw pellets.
      ;
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ), although 5 studies do not support this (
      • Van Putten G.
      Welfare in veal calf units.
      ;
      • De Wilt J.G.G.
      Behaviour and welfare of veal calves in relation to husbandry systems. PhD Thesis.
      ;
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      ;
      • Prevedello P.
      • Brscic M.
      • Schiavon E.
      • Cozzi G.
      • Gottardo F.
      Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
      ;
      • Webb L.E.
      • Van Reenen C.G.
      • Berends H.
      • Engel B.
      • De Boer I.J.M.
      • Gerrits W.J.J.
      • Bokkers E.A.M.
      The role of solid feed amount and composition and of milk replacer supply in veal calf welfare.
      ). The order of roughages from least to most deleterious appears to be hay < maize cob silage/beet pulp < lucerne < maize silage < straw (
      • Wensing T.
      • Breukink H.J.
      • Van Dijk S.
      The effect of feeding pellets of different types of roughage on the incidence of lesions in the abomasum of veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ;
      • Mattiello S.
      • Canali E.
      • Ferrante V.
      • Caniatti M.
      • Gottardo F.
      • Cozzi G.
      • Andrighetto I.
      • Verga M.
      The provision of solid feeds to veal calves: II. Behavior, physiology, and abomasal damage.
      ;
      • Räber R.
      • Kaufmann T.
      • Regula G.
      • Von Rotz A.
      • Stoffel M.H.
      • Posthaus H.
      • Rérat M.
      • Morel I.
      • Kirchhofer M.
      • Steiner A.
      • Bähler C.
      Effects of different types of solid feeds on health status and performance of Swiss veal calves. II. Basic feeding with whole milk.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). However, comparison between studies is difficult due to different amounts and particle sizes of roughage being fed. Interestingly,
      • Räber R.
      • Kaufmann T.
      • Regula G.
      • Von Rotz A.
      • Stoffel M.H.
      • Posthaus H.
      • Rérat M.
      • Kirchhofer M.
      • Steiner A.
      • Bähler C.
      Effects of different types of solid feeds on health status and performance of Swiss veal calves. I. Basic feeding with milk by-products.
      ,
      • Räber R.
      • Kaufmann T.
      • Regula G.
      • Von Rotz A.
      • Stoffel M.H.
      • Posthaus H.
      • Rérat M.
      • Morel I.
      • Kirchhofer M.
      • Steiner A.
      • Bähler C.
      Effects of different types of solid feeds on health status and performance of Swiss veal calves. II. Basic feeding with whole milk.
      ) 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 (
      • Räber R.
      • Kaufmann T.
      • Regula G.
      • Von Rotz A.
      • Stoffel M.H.
      • Posthaus H.
      • Rérat M.
      • Kirchhofer M.
      • Steiner A.
      • Bähler C.
      Effects of different types of solid feeds on health status and performance of Swiss veal calves. I. Basic feeding with milk by-products.
      ). In addition, one study compared 2 concentrate types, and found no difference in lesion incidence between them (
      • Räber R.
      • Kaufmann T.
      • Regula G.
      • Von Rotz A.
      • Stoffel M.H.
      • Posthaus H.
      • Rérat M.
      • Morel I.
      • Kirchhofer M.
      • Steiner A.
      • Bähler C.
      Effects of different types of solid feeds on health status and performance of Swiss veal calves. II. Basic feeding with whole milk.
      ). 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 (
      • Morisse J.P.
      • Huonnic D.
      • Cotte J.P.
      • Martrenchar A.
      The effect of four fibrous feed supplementations on different welfare traits in veal calves.
      ). Adding concentrate to roughage may prevent an increase in the lesion incidence that would normally happen with roughage (
      • Morisse J.P.
      • Cotte J.P.
      • Huonnic D.
      • Martrenchar A.
      Influence of dry feed supplements on different parameters of welfare in veal calves.
      ). However, some studies found no improvement or even a worsening of the damage with a combination of roughage and concentrate compared with only roughage (
      • Berends H.
      • Van Reenen C.G.
      • Stockhofe-Zurwieden N.
      • Gerrits W.J.J.
      Effects of early rumen development and solid feed composition on growth performance and abomasal health in veal calves.
      ;
      • Prevedello P.
      • Brscic M.
      • Schiavon E.
      • Cozzi G.
      • Gottardo F.
      Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
      ). Very high levels of concentrate (concentrate:roughage ≥80:20) have been seen to lead to acute ulceration in beef calves (
      • Tharwat M.
      • Ahmed A.F.
      Abomasal ulceration in buffaloes and cattle: Clinico-biochemical and pathological findings.
      ) and can increase abomasal damage in veal calves as the amount fed increases, even when MR is decreased simultaneously (
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      ). 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 (
      • Prevedello P.
      • Brscic M.
      • Schiavon E.
      • Cozzi G.
      • Gottardo F.
      Effects of the provision of large amounts of solid feeds to veal calves on growth and slaughter performance and intravitam and postmortem welfare indicators.
      ;
      • Brscic M.
      • Prevedello P.
      • Stefani A.L.
      • Cozzi G.
      • Gottardo F.
      Effects of the provision of solid feeds enriched with protein or nonprotein nitrogen on veal calf growth, welfare, and slaughter performance.
      ).

      Physical Form of Solid Feed

      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 (
      • Cozzi G.
      • Gottardo F.
      • Mutinelli F.
      • Contiero B.
      • Fregolent G.
      • Segato S.
      • Andrighetto I.
      Growth performance, behaviour, forestomach development and meat quality of veal calves provided with barley grain or ground wheat straw for welfare purpose.
      ). This implies that both the size and type of feed affect abomasal damage. In contrast,
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      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 (
      • Van Putten G.
      Welfare in veal calf units.
      ), which contradicts this hypothesis. In addition, pelleted maize silage was observed to cause more lesions than short-chopped or ground maize (cob) silage (
      • Wensing T.
      • Breukink H.J.
      • Van Dijk S.
      The effect of feeding pellets of different types of roughage on the incidence of lesions in the abomasum of veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ). 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 (
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). However, increasing amounts of cereal grains and straw were not seen to increase lesion incidence (
      • Morisse J.P.
      • Cotte J.P.
      • Huonnic D.
      • Martrenchar A.
      Influence of dry feed supplements on different parameters of welfare in veal calves.
      ), 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 (
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      ). 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;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). 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 (
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ,
      • Webb L.E.
      • Van Reenen C.G.
      • Berends H.
      • Engel B.
      • De Boer I.J.M.
      • Gerrits W.J.J.
      • Bokkers E.A.M.
      The role of solid feed amount and composition and of milk replacer supply in veal calf welfare.
      ). 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,
      • Prevedello P.
      • Brscic M.
      • Schiavon E.
      • Cozzi G.
      • Gottardo F.
      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 (
      • Berends H.
      • Van Reenen C.G.
      • Stockhofe-Zurwieden N.
      • Gerrits W.J.J.
      Effects of early rumen development and solid feed composition on growth performance and abomasal health in veal calves.
      ). 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 (
      • Jelinski M.D.
      • Ribble C.S.
      • Campbell J.R.
      • Janzen E.D.
      Descriptive epidemiology of fatal abomasal ulcers in Canadian beef calves.
      ;
      • Dirksen G.
      • Doll K.
      • Einhellig J.
      • Seitz A.
      • Rademacher G.
      • Breitner W.
      • Klee W.
      Abomasal ulcers in calves: Clinical investigations and experiences.
      ;
      • Vatn S.
      • Ulvund M.J.
      Abomasal bloat, haemorrhage and ulcers in young Norwegian lambs.
      ). Stimulating rumen fermentation and development at an early age has been proposed as a way of minimizing abomasal damage (
      • Berends H.
      • Van Reenen C.G.
      • Stockhofe-Zurwieden N.
      • Gerrits W.J.J.
      Effects of early rumen development and solid feed composition on growth performance and abomasal health in veal calves.
      ). 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 (
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      ;
      • Suarez-Mena F.X.
      • Heinrichs A.J.
      • Jones C.M.
      • Hill T.M.
      • Quigley J.D.
      Straw particle size in calf starters: Effects on digestive system development and rumen fermentation.
      ).
      In support of this theory, one study found that calves with better developed rumens had fewer abomasal lesions than calves with less developed rumens (
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ), and others found that stimulating early development with concentrate or hay meant that future feeding of coarse straw did not exacerbate damage (
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      ;
      • Webb L.E.
      • Van Reenen C.G.
      • Berends H.
      • Engel B.
      • De Boer I.J.M.
      • Gerrits W.J.J.
      • Bokkers E.A.M.
      The role of solid feed amount and composition and of milk replacer supply in veal calf welfare.
      ). 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 (
      • Berends H.
      • Van Reenen C.G.
      • Stockhofe-Zurwieden N.
      • Gerrits W.J.J.
      Effects of early rumen development and solid feed composition on growth performance and abomasal health in veal calves.
      ). 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 (
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      ), 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 (
      • Çatik S.
      • Akbala M.
      • Kurt H.
      • Salci H.
      Abomasal ulcer and jejunal ileus caused by trichobezoar in a two-day-old calf.
      ) that develop in the rumen and sometimes in the abomasum (
      • Osborne A.D.
      Hairballs in veal calves.
      ).
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      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 (
      • Morisse J.P.
      • Cotte J.P.
      • Huonnic D.
      • Martrenchar A.
      Influence of dry feed supplements on different parameters of welfare in veal calves.
      ,
      • Morisse J.P.
      • Huonnic D.
      • Cotte J.P.
      • Martrenchar A.
      The effect of four fibrous feed supplementations on different welfare traits in veal calves.
      ;
      • Cozzi G.
      • Gottardo F.
      • Mattiello S.
      • Canali E.
      • Scanziani E.
      • Verga M.
      • Andrighetto I.
      The provision of solid feeds to veal calves: I. Growth performance, forestomach development, and carcass and meat quality.
      ). Alternatively, calves fed SF may ingest less hair than calves fed MR only, as they display fewer abnormal oral behaviors (
      • Veissier I.
      • Ramirez de la Fe A.R.
      • Pradel P.
      Nonnutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions.
      ;
      • Mattiello S.
      • Canali E.
      • Ferrante V.
      • Caniatti M.
      • Gottardo F.
      • Cozzi G.
      • Andrighetto I.
      • Verga M.
      The provision of solid feeds to veal calves: II. Behavior, physiology, and abomasal damage.
      ), 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 (
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Van Reenen C.G.
      Comparing the effects of different roughage diets on grooming behaviour and hairball prevalence in veal calves.
      ,
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). Nevertheless,
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      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 (
      • Jelinski M.D.
      • Ribble C.S.
      • Campbell J.R.
      • Janzen E.D.
      Investigating the relationship between abomasal hairballs and perforating abomasal ulcers in unweaned beef calves.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Sasaki H.
      • Goyama T.
      • Noda Y.
      • Matsumoto K.
      • Kobayashi Y.
      • Inokuma H.
      Perforating abomasal ulcer caused by yolk sac tumor in a Holstein calf.
      ). Especially during abomasal surgeries performed on suckling calves, large amounts of hair were found in ulcerated or perforated abomasa (
      • Tulleners E.P.
      • Hamilton G.F.
      Surgical resection of perforated abomasal ulcers in calves.
      ;
      • Katchuik R.
      Abomasal disease in young beef calves: Surgical findings and management factors.
      ;
      • Çatik S.
      • Akbala M.
      • Kurt H.
      • Salci H.
      Abomasal ulcer and jejunal ileus caused by trichobezoar in a two-day-old calf.
      ). 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 (
      • Osborne A.D.
      Hairballs in veal calves.
      ). Studies in beef calves suggest that hairballs do not cause trauma to the abomasal mucosa and do not block the pylorus enough to cause ulceration (
      • Katchuik R.
      Abomasal disease in young beef calves: Surgical findings and management factors.
      ;
      • Jelinski M.D.
      • Ribble C.S.
      • Campbell J.R.
      • Janzen E.D.
      Investigating the relationship between abomasal hairballs and perforating abomasal ulcers in unweaned beef calves.
      ). In lambs, significantly more bezoars were found in lambs with abomasal ulcers than in those without ulcers (
      • Vatn S.
      • Ulvund M.J.
      Abomasal bloat, haemorrhage and ulcers in young Norwegian lambs.
      ). Despite these inconclusive results, veterinarians and researchers tend to assume a relationship between hairball presence in the abomasum and abomasal lesions (
      • Stokka G.
      • Perino L.
      The riddle of abomasal ulcers.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Çatik S.
      • Akbala M.
      • Kurt H.
      • Salci H.
      Abomasal ulcer and jejunal ileus caused by trichobezoar in a two-day-old calf.
      ).

      Nutrient Deficiencies

      Although it is often suggested that nutrient, most often mineral, deficiencies can cause or facilitate the formation of abomasal ulcers (
      • Jelinski M.D.
      • Ribble C.S.
      • Campbell J.R.
      • Janzen E.D.
      Investigating the relationship between abomasal hairballs and perforating abomasal ulcers in unweaned beef calves.
      ;
      • Stokka G.
      • Perino L.
      The riddle of abomasal ulcers.
      ;
      • Ahmed A.F.
      • Constable P.D.
      • Misk N.A.
      Effect of feeding frequency and route of administration on abomasal luminal pH in dairy calves fed milk replacer.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Van Immerseel F.
      • Pardon B.
      • Maes S.
      • Heyndrickx M.
      • Timbermont L.
      • Boyen F.
      • Haesebrouck F.
      • Ducatelle R.
      • Deprez P.
      Isolation of a clonal population of Clostridium perfringens type A from a Belgian Blue calf with abomasal ulceration.
      ), 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 (
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ). 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 (
      • Katchuik R.
      Abomasal disease in young beef calves: Surgical findings and management factors.
      ). 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 (
      • Mills K.W.
      • Johnson J.L.
      • Jensen R.L.
      • Woodard L.F.
      • Doster A.R.
      Laboratory findings associated with abomasal ulcers/tympany in range calves.
      ). Supplementation of copper to both cows and their calves immediately decreased the occurrence of ulceration close to zero (
      • Lilley C.W.
      • Hamar D.W.
      • Gerlach M.
      • Johnson J.L.
      Linking copper and bacteria with abomasal ulcers in beef calves.
      ).
      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 (
      • Lilley C.W.
      • Hamar D.W.
      • Gerlach M.
      • Johnson J.L.
      Linking copper and bacteria with abomasal ulcers in beef calves.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ). 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 (
      • Lilley C.W.
      • Hamar D.W.
      • Gerlach M.
      • Johnson J.L.
      Linking copper and bacteria with abomasal ulcers in beef calves.
      ;
      • Mills K.W.
      • Johnson J.L.
      • Jensen R.L.
      • Woodard L.F.
      • Doster A.R.
      Laboratory findings associated with abomasal ulcers/tympany in range calves.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ). 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 (
      • Hepola H.P.
      • Hänninen L.T.
      • Raussi S.M.
      • Pursiainen P.A.
      • Aarnikoivu A.-M.
      • Saloniemi H.S.
      Effects of providing water from a bucket or a nipple on the performance and behavior of calves fed ad libitum volumes of acidified milk replacer.
      ). Although some studies report that calves fed MR ad libitum drink hardly any water (
      • Hepola H.P.
      • Hänninen L.T.
      • Raussi S.M.
      • Pursiainen P.A.
      • Aarnikoivu A.-M.
      • Saloniemi H.S.
      Effects of providing water from a bucket or a nipple on the performance and behavior of calves fed ad libitum volumes of acidified milk replacer.
      ), others found that calves may ingest large amounts of up to 36 L/d, with an average consumption of 11.3 L/d (
      • Ruis-Heutinck L.
      • Van Reenen C.G.
      Wateropname door witvleeskalveren kan hoog oplopen.
      ;
      • Webb L.E.
      • Engel B.
      • Berends H.
      • Van Reenen C.G.
      • Gerrits W.J.J.
      • De Boer I.J.M.
      • Bokkers E.A.M.
      What do calves choose to eat and how do preferences affect behaviour?.
      ). Water intake increases when calves start consuming SF (
      • Kertz A.F.
      • Reutzel L.F.
      • Mahoney J.H.
      Ad libitum water intake by neonatal calves and its relationship to calf starter intake, weight gain, feces score, and season.
      ) and is higher in calves fed more SF (
      • Webb L.E.
      • Engel B.
      • Berends H.
      • Van Reenen C.G.
      • Gerrits W.J.J.
      • De Boer I.J.M.
      • Bokkers E.A.M.
      What do calves choose to eat and how do preferences affect behaviour?.
      ). Supplying calves with an increasing amount of free water (from 3 to 8 L/d) did not affect abomasal ulcers, erosions, or inflammations (
      • Gottardo F.
      • Mattiello S.
      • Cozzi G.
      • Canali E.
      • Scanziani E.
      • Ravarotto L.
      • Ferrante V.
      • Verga M.
      • Andrighetto I.
      The provision of drinking water to veal calves for welfare purposes.
      ). However, one risk assessment showed that calves receiving water ad libitum were at higher risk for lesions than those receiving none at all (
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ). 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:
      • Goldman H.
      • Rosoff C.B.
      Pathogenesis of acute gastric stress ulcers.
      ;
      • Weiner H.
      Use of animal models in peptic ulcer disease.
      ; guinea pig:
      • Ludwig W.M.
      • Lipkin M.
      Biochemical and cytological alterations in gastric mucosa of guinea pigs under restraint stress.
      ; piglet, but not pig:
      • Norton L.
      • Nolan P.
      • Sales J.E.
      • Eiseman B.
      A swine stress ulcer model.
      ). 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 (
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ). Therefore, many authors have noted that stress may be a predisposing or even causal factor for ulceration in calves as well (
      • Tulleners E.P.
      • Hamilton G.F.
      Surgical resection of perforated abomasal ulcers in calves.
      ;
      • Lourens J.M.
      • Van der Wal J.F.
      • Mouwen J.M.V.
      De maagslijmvliesbarrière en het alcus abomasi bij het mestkalf.
      ;
      • Wiepkema P.R.
      Over gedragsstoornissen bij dieren in de veehouderij.
      ;
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ;
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ;
      • Breukink H.J.
      • Wensing T.
      • Van Dijk S.
      • Mevius D.
      Effect of clenbuterol on the incidence of abomasal lesions in veal calves.
      ;
      • Mills K.W.
      • Johnson J.L.
      • Jensen R.L.
      • Woodard L.F.
      • Doster A.R.
      Laboratory findings associated with abomasal ulcers/tympany in range calves.
      ;
      • Lallès J.P.
      • Toullec R.
      Some aspects of nutrition and health in preruminant calves.
      ;
      • Stokka G.
      • Perino L.
      The riddle of abomasal ulcers.
      ;
      • Ahmed A.F.
      • Constable P.D.
      • Misk N.A.
      Effect of feeding frequency and route of administration on abomasal luminal pH in dairy calves fed milk replacer.
      ;
      • Constable P.D.
      • Ahmed A.F.
      • Misk N.A.
      Effect of suckling cow's milk or milk replacer on abomasal luminal pH in dairy calves.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Van Immerseel F.
      • Pardon B.
      • Maes S.
      • Heyndrickx M.
      • Timbermont L.
      • Boyen F.
      • Haesebrouck F.
      • Ducatelle R.
      • Deprez P.
      Isolation of a clonal population of Clostridium perfringens type A from a Belgian Blue calf with abomasal ulceration.
      ;
      • Sasaki H.
      • Goyama T.
      • Noda Y.
      • Matsumoto K.
      • Kobayashi Y.
      • Inokuma H.
      Perforating abomasal ulcer caused by yolk sac tumor in a Holstein calf.
      ;
      • Valgaeren B.R.
      • Pardon B.
      • Flahou B.
      • Verherstraeten S.
      • Goossens E.
      • Timbermont L.
      • Haesebrouck F.
      • Ducatelle R.
      • Van Immerseel F.
      • Deprez P.R.
      Prevalence and bacterial colonisation of fundic ulcerations in veal calves.
      ;
      • Webb L.E.
      • Bokkers E.A.M.
      • Heutinck L.F.M.
      • Engel B.
      • Buist W.G.
      • Rodenburg T.B.
      • Stockhofe-Zurwieden N.
      • Van Reenen C.G.
      Effects of roughage source, amount, and particle size on behavior and gastrointestinal health of veal calves.
      ;
      • Berends H.
      • Van den Borne J.J.G. C.
      • Mollenhorst H.
      • Van Reenen C.G.
      • Bokkers E.A.M.
      • Gerrits W.J.J.
      Utilization of roughages and concentrates relative to that of milk replacer increases strongly with age in veal calves.
      ;
      • Çatik S.
      • Akbala M.
      • Kurt H.
      • Salci H.
      Abomasal ulcer and jejunal ileus caused by trichobezoar in a two-day-old calf.
      ). 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 (
      • Weiner H.
      Use of animal models in peptic ulcer disease.
      ), 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 (
      • Weiner H.
      Use of animal models in peptic ulcer disease.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Kureljušić B.
      • Ivetić V.
      • Savić B.
      • Jezdimirović N.
      • Cvetojević D.
      • Kureljušić J.
      • Ilić Ž.
      • Stanojević S.
      • Stevančević M.
      Pathomorphological characteristics of abomasal ulcers in high-yielding dairy cows.
      ).
      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 (
      • Breukink H.J.
      • Wensing T.
      • Mouwen J.M.V. M.
      Abomasal ulcers in veal calves: Pathogenesis and prevention.
      ). 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.
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      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.
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      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 (
      • Veissier I.
      • Chazal P.
      • Pradel P.
      • Le Neindre P.
      Providing social contacts and objects for nibbling moderates reactivity and oral behaviors in veal calves.
      ;
      • Bokkers E.A.M.
      • Koene P.
      Activity, oral behaviour and slaughter data as welfare indicators in veal calves: A comparison of three housing systems.
      ), repeated regrouping (
      • Veissier I.
      • Boissy A.
      • DePassillé A.M.
      • Rushen J.
      • Van Reenen C.
      • Roussel S.
      • Andanson S.
      • Pradel P.
      Calves' responses to repeated social regrouping and relocation.
      ), or environmental enrichment (
      • Veissier I.
      • Chazal P.
      • Pradel P.
      • Le Neindre P.
      Providing social contacts and objects for nibbling moderates reactivity and oral behaviors in veal calves.
      ). 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 (
      • Lensink B.J.
      • Fernandez X.
      • Boivin X.
      • Pradel P.
      • Le Neindre P.
      • Veissier I.
      The impact of gentle contacts on ease of handling, welfare, and growth of calves and on quality of veal meat.
      ). 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 (
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ). 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 (
      • Webb L.E.
      Food for rumination—Developing novel feeding strategies to improve the welfare of veal calves.
      ). Stereotypies, such as these abnormal oral behaviors, are defined as repetitive and invariant behavioral patterns that lack an obvious goal or function (
      • Rushen J.
      • Mason G.
      A decade-or-more's progress in understanding stereotypic behaviour.
      ), and they may provide captive animals with a way to cope with a suboptimal environment (
      • Würbel H.
      • Bergeron R.
      • Cabib S.
      The coping hypothesis of stereotypic behaviour.
      ). 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 (
      • Weiner H.
      Use of animal models in peptic ulcer disease.
      ). 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 (
      • Ross J.G.
      Experimental infections of calves with the nematode parasite Ostertagia ostertagi.
      ;
      • Smith J.M.B.
      Letters to the editor: Candida infection in animals.
      ;
      • Stokka G.
      • Perino L.
      The riddle of abomasal ulcers.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ;
      • Moeller R.B.
      • Adaska J.
      • Reynolds J.
      • Blanchard P.C.
      Systemic bovine herpesvirus 1 infections in neonatal dairy 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 (
      • Overmier J.B.
      • Murison R.
      Restoring psychology's role in peptic ulcer.
      ). 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 (
      • Ross J.G.
      Experimental infections of calves with the nematode parasite Ostertagia ostertagi.
      ;
      • Ross J.G.
      • Dow C.
      The course and development of the abomasal lesions in calves experimentally infected with the nematode parasite Ostertagia ostertagi.
      ;
      • Snider T.G.
      • Williams J.C.
      • Sheehan D.S.
      • Fuselier R.H.
      Plasma pepsinogen, inhibited larval development, and abomasal lesions in experimental infections of calves with Ostertagia ostertagi.
      ,
      • Snider T.G.
      • Williams J.C.
      • Karns P.A.
      • Trammell H.E.
      • Romaire T.L.
      Synergistic influence of Ostertagia ostertagi and Trichostrongylus axei on Ostertagia ostertagi larvae inhibition and abomasal lesions in cattle.
      ;
      • Taylor L.M.
      • Parkins J.J.
      • Armour J.
      • Holmes P.H.
      • Bairden K.
      • Ibarra-Silva A.M.
      • Salman S.K.
      • McWilliam P.N.
      Pathophysiological and parasitological studies on Ostertagia ostertagi infections in calves.
      ;
      • Yang C.
      • Gibbs C.
      • Xiao L.
      • Wallace C.R.
      Prevention of pathophysiologic and immunomodulatory effects of gastrointestinal nematodiasis in calves by use of strategic anthelmintic treatments.
      ), cattle (
      • Snider T.G.
      • Williams J.C.
      • Karns P.A.
      • Trammell H.E.
      • Romaire T.L.
      Synergistic influence of Ostertagia ostertagi and Trichostrongylus axei on Ostertagia ostertagi larvae inhibition and abomasal lesions in cattle.
      ), and elk (
      • Woodbury M.R.
      • Parry N.M.A.
      Abomasal parasite syndrome in North American elk (Cervus elaphus canadensis).
      ), 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 (
      • Moeller R.B.
      • Adaska J.
      • Reynolds J.
      • Blanchard P.C.
      Systemic bovine herpesvirus 1 infections in neonatal dairy calves.
      ), beef calves (
      • Bianchi M.V.
      • Konradt G.
      • De Souza S.O.
      • Bassuino D.M.
      • Silveira S.
      • Mósena A.C.S.
      • Canal C.W.
      • Pavarini S.P.
      • Driemeier D.
      Natural outbreak of BVDV-1d–induced mucosal disease lacking intestinal lesions.
      ), and adult cattle (
      • Assis R.A.
      • Lobato F.C.F.
      • Facury Filho E.J.
      • Uzal F.A.
      • Santana F.J.F.
      • Dias L.D.
      • Parreiras M.
      Isolation of Clostridium perfringens type D from a suckling calve with ulcerative abomasitis.
      ), the prevalence of viral diseases is much lower than the prevalence of abomasal damage (2% compared with >70%;
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ;
      • Bianchi M.V.
      • Konradt G.
      • De Souza S.O.
      • Bassuino D.M.
      • Silveira S.
      • Mósena A.C.S.
      • Canal C.W.
      • Pavarini S.P.
      • Driemeier D.
      Natural outbreak of BVDV-1d–induced mucosal disease lacking intestinal lesions.
      ). 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 (
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ;
      • Mueller K.
      • Merrall M.
      • Sargison N.D.
      Left abomasal displacement and ulceration with perforation of abdominal musculature in two calves.
      ;
      • Sasaki H.
      • Goyama T.
      • Noda Y.
      • Matsumoto K.
      • Kobayashi Y.
      • Inokuma H.
      Perforating abomasal ulcer caused by yolk sac tumor in a Holstein calf.
      ) but are deemed irrelevant in veal calves.
      Table 2Evidence for the role of fungi in the etiology of abomasal damage in calves
      Study conclusionLesion typeFungus speciesNo. of calvesReferenceStudy type
      Observational.
      Isolation of fungal hyphae from damageNumerous ulcers, edemaNot identified3/5
      • Wray C.
      • Thomlinson J.R.
      Abomasal ulceration in calves.
      O
      Isolation of fungus from damageUlcerative abomasitisSaksenaea erythrospora1
      • Lawhon S.D.
      • Corapi W.V.
      • Hoffmann A.R.
      • Libal M.C.
      • Alvarez E.
      • Guarro J.
      • Wickes B.L.
      • Fu J.
      • Thompson E.H.
      • Sutton D.A.
      In utero infection of a calf by Saksenaea erythrospora resulting in neonatal abomasitis and dermatitis.
      O
      Isolation of fungal hyphae from damageUlcersAbsidia remosa Absidia corymbifera Mucor pusillus7
      • Gitter M.
      • Austwick P.K.C.
      The presence of fungi in abomasal ulcers of young calves: A report of seven cases.
      O
      1 Observational.
      Table 3Evidence for the role of bacteria in the etiology of abomasal damage in calves
      Study conclusionLesion typeBacterium speciesNo. of calves
      Veal calves unless otherwise specified.
      ReferenceStudy type
      O = observational; E = experimental.
      Isolation of bacteria from 6 calvesMany small (1–2 mm) ulcers: ulcerative abomasitisClostridium perfringens type D Escherichia coli (likely postmortem infection)6
      • Assis R.A.
      • Lobato F.C.F.
      • Facury Filho E.J.
      • Uzal F.A.
      • Santana F.J.F.
      • Dias L.D.
      • Parreiras M.
      Isolation of Clostridium perfringens type D from a suckling calve with ulcerative abomasitis.
      O
      No difference in bacteria incidence between damaged and intact abomasaType-1 ulcerAll215 fattening bulls, cows, and calves
      • Hund A.
      • Dzieciol M.
      • Schmitz-Esser S.
      • Wittek T.
      Characterization of mucosa-associated bacterial communities in abomasal ulcers by pyrosequencing.
      O
      No relation between bacteria and damageFundic type-1 ulcersC. perfringens Helicobacter spp.604
      • Valgaeren B.R.
      • Pardon B.
      • Flahou B.
      • Verherstraeten S.
      • Goossens E.
      • Timbermont L.
      • Haesebrouck F.
      • Ducatelle R.
      • Van Immerseel F.
      • Deprez P.R.
      Prevalence and bacterial colonisation of fundic ulcerations in veal calves.
      O
      No relation between bacteria and damageFundic and pyloric ulcers and erosionsE. coli Streptococcus faecalis Streptococcus bovis Bacillus spp. Corynebacterium spp. Moraxella spp. Acinetobacter spp.304
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      O
      Bacteria likely postmortem contaminantFatal ulcersC. perfringens type A30 beef calves
      • Jelinski M.D.
      • Ribble C.S.
      • Chirino-Trejo M.
      • Clark E.G.
      • Janzen E.D.
      The relationship between the presence of Helicobacter pylori, Clostridium perfringens type A, Campylobacter spp., or fungi and fatal abomasal ulcers in unweaned beef calves.
      O
      Isolation of bacteria from one calfHundreds of small type-1 ulcersC. perfringens1
      • Van Immerseel F.
      • Pardon B.
      • Maes S.
      • Heyndrickx M.
      • Timbermont L.
      • Boyen F.
      • Haesebrouck F.
      • Ducatelle R.
      • Deprez P.
      Isolation of a clonal population of Clostridium perfringens type A from a Belgian Blue calf with abomasal ulceration.
      O
      Isolation of bacteria from one calfMany small ulcers: ulcerative abomasitisC. perfringens type A1 Asian gaur calf
      • Songer J.G.
      • Miskimins D.W.
      Clostridial abomasitis in calves: Case report and review of the literature.
      O
      Administration of bacteria caused damageUlcerative abomasitisC. perfringens type A10 bull calves
      • Roeder B.L.
      • Chengappa M.M.
      • Nagaraja T.G.
      • Avery T.B.
      • Kennedy G.A.
      Experimental induction of abdominal tympany, abomasitis, and abomasal ulceration by intraruminal inoculation of Clostridium perfringens type A in neonatal calves.
      E
      Administration of bacteria caused damageGross lesions, abomasitis and sometimes peritonitisSalmonella enterica6
      • Carlson S.A.
      • Stoffregen W.C.
      • Bolin S.R.
      Abomasitis associated with multiple antibiotic resistant Salmonella enterica serotype Typhimurium phagetype DT104.
      E
      Administration of bacteria caused damageGross lesions throughout the gastrointestinal tractChlamydiae strain LW-61312
      • Doughri A.M.
      • Young S.
      • Storz J.
      Pathological changes in intestinal chlamydial infection of newborn calves.
      E
      1 Veal calves unless otherwise specified.
      2 O = observational; E = experimental.
      Table 4Evidence for the role of parasites in the etiology of abomasal damage in calves
      Study conclusionLesion typeParasite speciesNo. of calvesReferenceStudy type
      E = experimental.
      Administration of parasite caused damageAbomasitis with ulcersOstertagia ostertagi27
      • Ross J.G.
      Experimental infections of calves with the nematode parasite Ostertagia ostertagi.
      E
      Administration of parasite caused damageLarvae-containing nodules, edemaO. ostertagi10
      • Ross J.G.
      • Dow C.
      The course and development of the abomasal lesions in calves experimentally infected with the nematode parasite Ostertagia ostertagi.
      E
      Administration of parasite caused damageSmall nodulesO. ostertagi10
      • Snider T.G.
      • Williams J.C.
      • Sheehan D.S.
      • Fuselier R.H.
      Plasma pepsinogen, inhibited larval development, and abomasal lesions in experimental infections of calves with Ostertagia ostertagi.
      E
      Administration of parasite caused damageSmall nodulesO. ostertagi, Trichostrongylus axei, or both20
      • Snider T.G.
      • Williams J.C.
      • Karns P.A.
      • Trammell H.E.
      • Romaire T.L.
      Synergistic influence of Ostertagia ostertagi and Trichostrongylus axei on Ostertagia ostertagi larvae inhibition and abomasal lesions in cattle.
      E
      Administration of parasite caused damageFundic and pyloric nodulesO. ostertagi25
      • Taylor L.M.
      • Parkins J.J.
      • Armour J.
      • Holmes P.H.
      • Bairden K.
      • Ibarra-Silva A.M.
      • Salman S.K.
      • McWilliam P.N.
      Pathophysiological and parasitological studies on Ostertagia ostertagi infections in calves.
      E
      Administration of parasite caused damageNodulesO. ostertagi and Cooperia oncophora24
      • Yang C.
      • Gibbs C.
      • Xiao L.
      • Wallace C.R.
      Prevention of pathophysiologic and immunomodulatory effects of gastrointestinal nematodiasis in calves by use of strategic anthelmintic treatments.
      E
      1 E = experimental.
      Table 5Evidence for the role of viruses in the etiology of abomasal damage in calves
      Study conclusionLesion typeVirus speciesNo. of calvesReferenceStudy type
      O = observational.
      Viral infection caused lesions in various organs, including the abomasumUlcers, edemaBovine herpesvirus 12/62 calves showed ulcers in the abomasum
      • Moeller R.B.
      • Adaska J.
      • Reynolds J.
      • Blanchard P.C.
      Systemic bovine herpesvirus 1 infections in neonatal dairy calves.
      O
      Viral infection caused lesions in various organs, including the abomasumUlcersBovine viral diarrhea virus1/7 calves showed ulcers in the abomasum
      • Bianchi M.V.
      • Konradt G.
      • De Souza S.O.
      • Bassuino D.M.
      • Silveira S.
      • Mósena A.C.S.
      • Canal C.W.
      • Pavarini S.P.
      • Driemeier D.
      Natural outbreak of BVDV-1d–induced mucosal disease lacking intestinal lesions.
      O
      1 O = observational.

      Medication

      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.

      ;
      • Pardon B.
      • Catry B.
      • Dewulf J.
      • Persoons D.
      • Hostens M.
      • De Bleecker K.
      • Deprez P.
      Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves.
      ), 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 (
      • Pardon B.
      • Catry B.
      • Dewulf J.
      • Persoons D.
      • Hostens M.
      • De Bleecker K.
      • Deprez P.
      Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves.
      ). 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 (
      • Pardon B.
      • Catry B.
      • Dewulf J.
      • Persoons D.
      • Hostens M.
      • De Bleecker K.
      • Deprez P.
      Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves.
      ). Compared with the 40% use of AM drugs, NSAID were given to 0.6% of veal calves per day of production in Belgium (
      • Pardon B.
      • Catry B.
      • Dewulf J.
      • Persoons D.
      • Hostens M.
      • De Bleecker K.
      • Deprez P.
      Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves.
      ). Most NSAID are likely given as part of the treatment for respiratory diseases, similar to AM drugs (
      • Pardon B.
      • Catry B.
      • Dewulf J.
      • Persoons D.
      • Hostens M.
      • De Bleecker K.
      • Deprez P.
      Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves.
      ). Ibuprofen (
      • Walsh P.
      • Carvallo Chaigneau F.R.
      • Anderson M.
      • Behrens N.
      • McEligot H.
      • Gunnarson B.
      • Gershwin L.J.
      Adverse effects of a 10-day course of ibuprofen in Holstein calves.
      ) and other NSAID (
      • Semrad S.D.
      • Dubielzig R.
      Effect of repeated administration of tirilazad mesylate on healthy and endotoxemic calves: A pilot study.
      ;
      • Sasaki H.
      • Goyama T.
      • Noda Y.
      • Matsumoto K.
      • Kobayashi Y.
      • Inokuma H.
      Perforating abomasal ulcer caused by yolk sac tumor in a Holstein calf.
      ) have been found to cause abomasal lesions in calves. Additionally, NSAID are a known cause of peptic ulcers in humans (
      • Yeomans N.D.
      • Næsdal J.
      Systematic review: Ulcer definition in NSAID ulcer prevention trials.
      ). 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 (
      • Veissier I.
      • Chazal P.
      • Pradel P.
      • Le Neindre P.
      Providing social contacts and objects for nibbling moderates reactivity and oral behaviors in veal calves.
      ). 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
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
      and
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      , 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 (
      • Smith D.F.
      • Munson L.
      • Erb H.N.
      Abomasal ulcer disease in adult dairy cattle.
      ;
      • Sanford S.E.
      • Josephson G.K.A.
      Perforated abomasal ulcers in post-parturient Jersey cows.
      ;
      • Ok M.
      • Sen I.
      • Turgut K.
      • Irmak K.
      Plasma gastrin activity and the diagnosis of bleeding abomasal ulcers in cattle.
      ;
      • Tharwat M.
      • Ahmed A.F.
      Abomasal ulceration in buffaloes and cattle: Clinico-biochemical and pathological findings.
      ). In beef calves, bad weather has often been proposed as a contributing factor (
      • Jensen R.
      • Pierson R.E.
      • Braddy P.M.
      • Saari D.A.
      • Benitez A.
      • Lauerman L.H.
      • Horton D.P.
      • McChesney A.E.
      Fetal abomasal ulcers in yearling feedlot cattle.
      ;
      • Lilley C.W.
      • Hamar D.W.
      • Gerlach M.
      • Johnson J.L.
      Linking copper and bacteria with abomasal ulcers in beef calves.
      ;
      • Mills K.W.
      • Johnson J.L.
      • Jensen R.L.
      • Woodard L.F.
      • Doster A.R.
      Laboratory findings associated with abomasal ulcers/tympany in range calves.
      ;
      • Marshall T.S.
      Abomasal ulceration and tympany of calves.
      ). 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 (
      • Jelinski M.D.
      • Ribble C.S.
      • Campbell J.R.
      • Janzen E.D.
      Descriptive epidemiology of fatal abomasal ulcers in Canadian beef calves.
      ).
      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
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      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 (
      • Weiner H.
      Use of animal models in peptic ulcer disease.
      ). 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 (
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      ). Calves living in a stable with an open-front building had fewer pyloric lesions than those in stables with manual ventilation (
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      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 (
      • Wensing T.
      • Breukink H.J.
      • Van Dijk S.
      The effect of feeding pellets of different types of roughage on the incidence of lesions in the abomasum of veal calves.
      ;
      • Wiepkema P.R.
      • Van Hellemond K.K.
      • Roessingh P.
      • Romberg H.
      Behaviour and abomasal damage in individual veal calves.
      ), although contradictory findings exist (
      • Räber R.
      • Kaufmann T.
      • Regula G.
      • Von Rotz A.
      • Stoffel M.H.
      • Posthaus H.
      • Rérat M.
      • Morel I.
      • Kirchhofer M.
      • Steiner A.
      • Bähler C.
      Effects of different types of solid feeds on health status and performance of Swiss veal calves. II. Basic feeding with whole milk.
      ). 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 (
      • Welchman D.D.
      • Baust G.N.
      A survey of abomasal ulceration in veal calves.
      ), 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 (
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
      ), although this was not seen in fattening bulls, in which carcass weight and fat distribution were not found to affect abomasal ulceration (
      • Hund A.
      • Beer T.
      • Wittek T.
      Abomasal ulcers in slaughtered cattle in Austria.
      ). 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 (
      • Webb L.E.
      • Engel B.
      • Berends H.
      • Van Reenen C.G.
      • Gerrits W.J.J.
      • De Boer I.J.M.
      • Bokkers E.A.M.
      What do calves choose to eat and how do preferences affect behaviour?.
      ).
      In humans, stomach ulcers are thought to have a heritable component (
      • Holle G.E.
      Pathophysioogy and modern treatment of ulcer disease.
      ). 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.
      FactorForAgainstSummary of findingsImportant
      Milk replacer (MR)42Despite little actual experimental study in this field, MR is likely to play an important role. The exact pathways are unknown.Yes
      Solid feed92Solid feed provision on top of MR is likely to affect the level of damage, unless roughage is provided ad libitum.Yes
      Rumen development31The 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
      Hairballs01Both hairballs in the rumen and abomasum do not show a clear association with abomasal lesions.No
      Nutrients01Only iron was tested in veal calves.No
      Water1
      A cross-country survey by Brscic et al. (2011), where water provision was correlated with solid feed provision.
      1The experimental study against has stronger findings than the observational study, which involves confounders.Unlikely
      Stress1
      Substantial confounding factor of nutrition (Bähler et al., 2010).
      4Despite 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.Unlikely
      Bacteria3
      Two of these studies found damage very different from that commonly found in veal calf abomasa.
      3Studies 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
      Viruses00No 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
      Fungi00No research in veal calves.Unknown
      Parasites00No 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
      Breed12Breed is probably only relevant when it affects growth rate: hence feeding speed and amounts ingested.Unknown
      Medication01Too little medication specifically tested. Medication is widespread enough to be linked to damage.Unknown
      Season10Too little work on this. Probably only has an indirect effect.Unknown
      Housing20Too little work on this. Probably only has an indirect effect.Unknown
      Growth rate10Although there is little work on this, our own unpublished work suggests that calves that grow faster have more damage.Yes
      Genetics00No study.Unknown
      1 Only studies specifically studying veal calves are included here.
      2 A cross-country survey by
      • Brscic M.
      • Heutinck L.F.M.
      • Wolthuis-Fillerup M.
      • Stockhofe N.
      • Engel B.
      • Visser E.K.
      • Gottardo F.
      • Bokkers E.A.M.
      • Lensink B.J.
      • Cozzi G.
      • Van Reenen C.G.
      Prevalence of gastrointestinal disorders recorded at postmortem inspection in white veal calves and associated risk factors.
      , where water provision was correlated with solid feed provision.
      3 Substantial confounding factor of nutrition (
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      Effects of the two production programs “Naturafarm” and “conventional” on the prevalence of non-perforating abomasal lesions in Swiss veal calves at slaughter.
      ).
      4 Two of these studies found damage very different from that commonly found in veal calf abomasa.
      Figure thumbnail gr1
      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 (
      • Constable P.D.
      • Wittek T.
      • Ahmed A.F.
      • Marshall T.S.
      • Sen I.
      • Nouri M.
      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.
      ) and in humans, peptic ulcer disease has been associated with delayed gastric emptying (
      • Minami H.
      • McCallum R.W.
      The physiology and pathophysiology of gastric emptying in humans.
      ). 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 (
      • Bähler C.
      • Regula G.
      • Stoffel M.H.
      • Steiner A.
      • Von Rotz A.
      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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