Effect of Feeding Frequency and Route of Administration on Abomasal Luminal pH in Dairy Calves Fed Milk Replacer1

J. Dairy Sci. 85:1502–1508  American Dairy Science Association, 2002.

Effect of Feeding Frequency and Route of Administration on Abomasal Luminal pH in Dairy Calves Fed Milk Replacer1 A. F. Ahmed,* P. D. Constable,† and N. A. Misk‡ *Department of Veterinary Surgery, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt †Department of Veterinary Clinical Medicine, University of Illinois, 1008 W. Hazelwood, Urbana, IL 61802 ‡Department of Veterinary Surgery, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt

ABSTRACT The aim of this study was to determine the effect of feeding frequency and route of administration on abomasal luminal pH in suckling calves. Six male dairy calves with cannulae in the abomasal body were administered the following six treatments in a randomized crossover design: 24 h fasting, suckling of a high-quality milk replacer (all-milk protein; 12% of body weight [BW]/d) at 12-h (2x), 8-h (3x), 6-h (4x), and 3-h (8x) intervals, and ruminal intubation of milk replacer (12% of body weight/day) at a 12-h (2x) interval. Abomasal luminal pH was measured every second for 24 h with miniature glass pH electrodes. Least squares mean 24h fasting abomasal luminal pH was 1.73, whereas mean 24-h pH after suckling and intubation of milk replacer every 12 h were higher at 3.44 and 3.17, respectively. Increasing the frequency of milk replacer suckling to 3x, 4x, and 8x increased mean 24-h abomasal luminal pH; however, there was no difference in mean 24-h pH between 3x (3.69), 4x (3.64), and 8x (3.67) suckling. The percentage of the 24-h recording period that abomasal luminal pH was > 3.0 was 0, 49, 53, 61, 61, and 71% for fasting, 2x intubation of milk replacer, and 2x, 3x, 4x, and 8x suckling of milk replacer, respectively. Increasing the frequency of milk replacer suckling may be efficacious in the prophylaxis of abomasal ulceration in milk-fed calves. (Key words: calf, feeding frequency, milk replacer, abomasal ulceration) INTRODUCTION Abomasal ulceration occurs commonly in calves but less frequently in adult cattle, with a prevalence of 5

Received October 10, 2001. Accepted December 12, 2001. Corresponding author: P. D. Constable; e-mail: p-constable@ uiuc.edu. 1 Funded by the Cultural and Educational Bureau, Embassy of the Arab Republic of Egypt. This report represents a portion of the thesis submitted by the senior author to the graduate school of Assiut University as partial fulfillment of the requirement for the Ph.D. degree (work done at the University of Illinois).

to 76 (Mei, 1985), 32 (Wensing et al., 1986), 45 (Wiepkema et al., 1987), 57 (Breukink et al., 1989), 75 (Welchman and Baust, 1987), and 76% (Groth and Berner, 1971) in healthy veal calves, 1.0 (Aukema and Breukink, 1974) to 2.6% (Hemmingsen, 1966) in healthy dairy cows, 1.8% in healthy beef cows (Jensen et al., 1954), and 1.6% in feedlot cattle (Jensen et al., 1976). Abomasal ulceration is also a common cause of death in suckling beef calves aged 1 to 2 mo old in the north central region of the United States and along the eastern slopes of the Rocky Mountains in Canada (Tulleners and Hamilton, 1980; Mills et al., 1990; Jelinski et al., 1995), with cases occurring more frequently during or after a period of inclement weather (Tulleners and Hamilton, 1980; Lilley et al., 1985; Mills et al., 1990). The cause for the high prevalence of abomasal ulceration among suckling calves is unknown (Van Putten, 1982), although diet has been suspected to play an important role in the etiopathogenesis (Mei, 1985; Dirksen, 1994). Despite the recent changes in veal calf husbandry, the observation by Tantz (1912) that veal calves frequently have abomasal ulcers when slaughtered at 8 to 14 wk of age supports the concept that diet is the main cause for ulcer development in milk-fed calves (Wiepkema et al., 1987). Four main etiologies have been proposed for abomasal ulceration in suckling calves: 1) mechanical abrasion of the pyloric antrum due to ingestion of coarse roughage, such as straw, or the presence of trichobezoars; 2) infection with bacteria such as Clostridium perfringens type A or unidentified fungi; 3) trace mineral deficiencies; and 4) concurrent stress (Roeder et al., 1987; Mills et al., 1990). None of these factors or theories alone adequately explains abomasal ulcer formation in suckling calves (Jelinski et al., 1995). In an attempt to develop an effective and practical medical treatment for abomasal ulceration in suckling calves, we developed a method for the continuous measurement of abomasal luminal pH and completed a series of studies examining the effect of orally administered cimetidine, ranitidine and Al(OH)3/Mg(OH)2 on abomasal luminal pH in milk-fed dairy calves (Ahmed et al., 2001, 2002). The results of these studies indicated

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that preprandial abomasal luminal pH in suckling dairy calves was low (mean 1.4), and that suckling milk replacer at 12% BW/d divided into two feedings resulted in sustained periods of low luminal pH (Ahmed et al., 2001, 2002). Abomasal hyperacidity is considered to play an important role in the pathogenesis of abomasal ulceration in adult cattle, as back diffusion of hydrogen ions from the lumen into the mucosa permits penetration of the proteolytic enzyme pepsin into the deeper layers of the abomasal mucosa, leading to further damage and ulceration (Whitlock, 1980). Because sustained periods of decreased luminal pH increase the likelihood of injury to the abomasal mucosa, we hypothesized that feeding frequency would have a profound effect on mean 24-h luminal pH in calves fed milk replacer and thereby influence the risk of abomasal ulceration. The aim of this study was, therefore, to determine the effect of feeding frequency and route of administration on abomasal luminal pH in suckling calves. MATERIALS AND METHODS Animals The University of Illinois Laboratory Animal Care and Use Committee approved this study. Six male colostrum-fed healthy dairy calves (five Holstein-Friesian, one Ayrshire) were surgically instrumented with an abomasal body cannula at 3 d of age as previously described (Ahmed et al., 2001, 2002). Experimental Design Beginning on d 5 of life (mean BW 43 kg, range 35 to 48 kg), each calf was subjected to six treatments in a Latin square design (all calves received all treatments in random order), and abomasal luminal pH was monitored continuously for at least 24 h, starting at 7:15 a.m. Calves had access to fresh water at all times. A 24h washout period was used between treatments; during this washout period calves suckled a high-quality milk replacer (all-milk protein; Supreme All Milk, Calf Milk Replacer, AGRIMASTER, Janesville, WI; 12% of BW/ d) at 12-h intervals. The milk replacer contained CP, ≥ 22%; crude fat, ≥ 20%; crude fiber, ≤ 0.15%; calcium, ≥ 0.50%; phosphorus, ≥ 1.00%. The protein source was dried whey, dried whey product, dried milk protein, and dried skim milk in unstated proportions. Milk replacer powder was dissolved in water at approximately 37°C at 120 g/L (4 oz/quart) and administered by a bottle with a nipple at 7:30 a.m. and 7:30 p.m. The six treatments were fasting 24 h, ruminal intubation of milk replacer (12% of BW/d) at 12-h intervals, and suckling of milk replacer (12% of BW/d) at 12-h (2x), 8-h (3x), 6h (4x), and 3-h (8x) intervals. Milk replacer adminis-

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tered by intubation or suckling was prepared as stated during the washout period. Abomasal pH Measurement A miniature glass pH electrode (M3 internal reference glass pH electrode, Medical Instruments Corporation, Solothurn, Switzerland) was advanced through a 6-cm-long rubber tube (outside diameter, 12 mm; inside diameter, 7 mm) containing a silastic plug with a small central hole at the proximal end to minimize electrode migration. The pH electrode was then advanced through the cannula to protrude 5 mm into the abomasal lumen. The electrode was secured to the cannula by placing the distal end of the rubber tube over the outside of the cannula. The glass pH electrode was connected to a pH meter (Cole-Parmer pH/mV/Rel mV/°C Benchtop Meter, Cole-Parmer Instrument Co., Vernon Hills, IL) that was connected to an analog-to-digital board (CODAS, Dataq Instruments, Inc., Akron, OH), the electrical signal was digitized at 1 Hz, and the data stored on the hard disk of a personal computer. The pH electrode was calibrated immediately before insertion and after removal against reference buffer solutions of pH 2.0 and 7.0 at 20°C. During offline data analysis, abomasal pH was smoothed using a 60-point moving average and the lowest smoothed pH value for each minute used as the pH value for that minute. The smoothing procedure minimized recording artifacts that occurred when the pH probe transiently contacted the abomasal mucosa due to changes in the calf’s position or contraction of the abomasum. Statistical Analysis Data were expressed as least squares means (± SEM), and significance was P < 0.05. The two variables examined to measure the effect of treatment (different feeding frequency or route of administration) on abomasal luminal acidity were mean 24-h pH and the pH-threshold curve. Mean 24-h pH and pH-threshold curves were developed using pH values from time = 1 min to time = 24 h in 1-min intervals; this provided 1440 data points for each 24-h recording period. The pH-threshold curve was obtained by calculating the percentage of the 24h period that pH was > 0 to > 6.0 in 0.5-unit increments. The effects of treatment on mean 24 h pH and percentage of the 24-h period that pH was > 3.0 and > 4.0 were evaluated using repeated measures ANOVA (SAS, 1988). Least squares means were calculated and compared using Bonferroni adjusted P values. Luminal pH cut points of 3.0 and 4.0 were selected for comparison because a pH > 3.0 and > 4.0 is accompanied by a slower Journal of Dairy Science Vol. 85, No. 6, 2002

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AHMED ET AL. Table 1. Least squares means for 24-h abomasal luminal pH of dairy calves (n = 6) administered different treatments. Treatment

Item measured

Suckled 2x

Mean pH % 24 h that pH >3.0 % 24 h that pH >4.0

a

3.44 53ab 46a

Intubated 2x b

3.17 49a 31b

Fasted c

1.73 0c 0c

Suckled 3x

Suckled 4x

Suckled 8x

d

d

d

3.69 61bd 51a

3.64 61bd 52a

3.67 71d 48a

SE 0.12 9 9

Means with different superscripts were significantly (P < 0.05) different.

a–d

activation rate of pepsinogen and prochymosin, respectively, and pepsin and chymosin are the most important proteolytic enzymes in the abomasum of the milk-fed calf (Henschel, 1973; Pedersen et al., 1979). To reduce the size of the dataset to facilitate repeated measures ANOVA, a five-point moving average was applied to the pH values at each minute and a smaller dataset extracted that contained smoothed luminal pH values at 15-min intervals; this reduced the size of the dataset from 1440 to 96 data points for each 24-h recording period. The effects of treatment and time on the smoothed luminal pH values were then evaluated using repeated measures ANOVA, with repeated measures on both treatment and time (SAS, 1988). Least squares means for the different levels of each factor were calculated, and Bonferroni adjusted P values were used to compare smoothed luminal pH values at each 15-min time interval (15 min to 24 h) to that obtained during the pretreatment period. Least squares mean pH values at time = −15 and 0 min were depicted graphically but were not included in the statistical analysis.

Abomasal pH remained constant below 2.0 during 24 h fasting (Figure 1) with least squares mean 24-h pH of 1.73 (Table 1). When milk replacer was suckled every 12 h (2x), abomasal luminal pH increased from a baseline value of 1.4 to 6.0 within 3 min, remained constant for 2 h, then decreased to the preprandial value by 8 h after feeding. Abomasal luminal pH was constant from 8 h to 12 h, and increased again after the second feeding of milk replacer at 12 h. Abomasal pH increased rapidly to 6.0 after intubation of milk replacer but decreased faster than that with 2x suckling milk (Figure 1). Mean 24-h pH during 2x suckling was higher than that obtained during intubation of milk replacer (Table 1). Abomasal pH increased rapidly to 6.0 after suckling milk replacer every 8 h (3x), remained constant for 1 to 1.5 h, then gradually decreased to preprandial pH within 6 h, remained constant for 2 h, and then increased similarly after the second and third feedings (Figure 2). Suckling milk replacer administered every

RESULTS Animals Abomasal cannulae were well tolerated by all calves, with maintenance of appetite, a mean increase in BW of 2.5 kg (range, 2.0 to 3.0 kg), and no episodes of pyrexia (as assessed by rectal temperature) during the study period. The mean time taken to administer the allotted volume of milk replacer was 5, 4, 2, and 1 min for 2x, 3x, 4x, and 8x suckling, respectively, and 3 min for 2x intubation of milk replacer. Abomasal pH Measurement Electrode drift during the 24-h recording period was +0.04 (range −0.16 to +0.11) for buffer pH 2.00 and +0.07 (range 0.00 to +0.15) for buffer pH 7.00. Raw pH values were used for statistical analysis because of the minimal drift. Journal of Dairy Science Vol. 85, No. 6, 2002

Figure 1. Least squares mean abomasal luminal pH in dairy calves (n = 6) that were fasted for 24 h (—), intubated with milk replacer 2x (䊊–䊊), or allowed to suckle milk replacer 2x ( ). Open symbols (2x intubation of milk replacer) and closed symbols (24 h fasting) at the top of the graph represent values that were significantly (P < 0.05) different from those for 2x suckling of milk replacer at the same time. Bar represents the overall standard error (SE) for least squares means.

FEEDING FREQUENCY AND ABOMASAL PH IN CALVES

Figure 2. Least squares mean abomasal luminal pH in dairy calves (n = 6) that suckled milk replacer at 8-h intervals (3x; 䊊–䊊) ). Open symbols at the top of the graph and 12-h intervals (2x; represent mean values that were significantly (P < 0.05) different at the same time. Bar represents the overall standard error (SE) for least squares means.

6 h (4x) increased abomasal pH to 5.5 within 3 min; pH remained constant for approximately 1 h before gradually decreasing to the preprandial value by 5 h. Abomasal pH changed similarly after the second, third, and fourth feedings (Figure 3). Suckling milk replacer administered every 3 h (8x) increased abomasal pH to 5.0; pH remained constant for approximately 45 min before decreasing to 2.0 by 3 h. Abomasal pH changed similarly after the second through eighth feedings (Fig-

Figure 3. Least squares mean abomasal luminal pH in dairy calves (n = 6) that suckled milk replacer at 6-h intervals (4x; 䊊–䊊) and 12-h intervals (2x; ). Open symbols at the top of the graph represent mean values that were significantly (P < 0.05) different at the same time. Bar represents the overall standard error (SE) for least squares means.

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Figure 4. Least squares mean abomasal luminal pH in dairy calves (n = 6) that suckled milk replacer at 3-h intervals (8x; 䊊–䊊) ). Open symbols at the top of the graph and 12-h intervals (2x; represent values that were significantly (P < 0.05) different at the same time. Bar represents the overall standard error (SE) for least squares means.

ure 4). Mean 24-h pH for 3x, 4x, and 8x suckling of milk replacer were similar but were higher than that for 2x suckling (Table 1). The pH threshold curves (Figures 5 and 6) indicated that compared to suckling milk replacer every 12 h (2x), the percentage of the 24 h period that abomasal luminal pH >3.0 was lower for fasting calves and higher for calves suckling every 3 h (8x; Table 1). Compared to

Figure 5. Least squares mean abomasal luminal pH-threshold curves in dairy calves (n = 6) that were fasted for 24 h, intubated at 12-h intervals (Tubed 2x) with milk replacer, and suckled milk replacer at 12-h intervals (Suckled 2x). Each data point represents the percentage of the 24-h recording period that abomasal pH exceeded the stated pH threshold value. Bar represents the overall standard error (SE) for least squares means. Journal of Dairy Science Vol. 85, No. 6, 2002

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Figure 6. Least squares mean abomasal luminal pH-threshold curves in dairy calves (n = 6) that suckled milk replacer at 12-h intervals (2x), 8-h intervals (3x), 6-h intervals (4x), and 3-h intervals (8x). Each data point represents the percentage of the 24-h recording period that abomasal pH exceeded the stated pH threshold value. Bar represents the overall standard error (SE) for least squares means.

suckling milk replacer administered every 12 h (2x), the percentage of the 24-h period that pH >4.0 was lower for fasting and 2x intubation of milk replacer (Table 1). DISCUSSION This appears to be the first report of the effect of feeding frequency and route of administration on abomasal luminal pH in suckling calves. Major findings of the study reported here were 1) mean 24-h pH during fasting was low (1.73), 2) mean 24-h pH after suckling and intubation of milk replacer twice a day were 3.44 and 3.17, respectively, 3) increasing the frequency of milk replacer suckling to more than twice a day increased mean 24-h abomasal pH, with no difference in mean 24-h pH between 3x, 4x, and 8x suckling of milk replacer. Beef calves usually suckle three to six meals per 24 h (range 1 to 11 meals per 24 h [Walker, 1962; Hafez and Lineweaver, 1968; Odde et al., 1985]), and ad libitum suckling and twice-daily bucket feeding produce similar rates of feed consumption and growth rate (Kaufhold et al., 2000). Feeding two, three, or four meals daily of acidified milk replacer does not alter live-weight gain, heat production, or energy retention in dairy calves (Williams et al., 1986) and there is no difference in total feed consumption, weight gain, and diarrhea incidence between twice-daily suckling and ad libitum feeding in dairy calves (Medvecky, 1983). It therefore appears that increasing the suckling frequency in dairy calves above Journal of Dairy Science Vol. 85, No. 6, 2002

the industry standard of every 12 h will more closely reflect suckling behavior in beef calves, not adversely affect growth rate, and may decrease the prevalence of abomasal ulceration by increasing mean 24-h luminal pH and percentage of the 24-h period that luminal pH > 3.0. An important goal when preventing abomasal ulceration in milk-fed calves is presumably to increase luminal pH and thereby inhibit the proteolytic activity of pepsin and chymosin. Chymosin is the major proteinase present at birth in calves, but pepsinogen secretion occurs at or soon after birth (Henschel, 1973) and is quantitatively more important than chymosin for proteolysis after d 17 of life (Williams et al., 1976). Bovine pepsinogen is activated when pH ≤ 5.0; the optimal pH for activation is 2.0 to 2.5 (Berghen et al., 1987; Henschel, 1973), but a slow activation rate is present whenever pH ≥ 3.0 (Glogowski and Rand, 1978). Bovine chymosin has an optimal pH for activation of 3.0 to 3.8 (Henschel, 1973; Williams et al., 1976; Pedersen et al., 1979), with a rapid increase in activation rate as pH decreases below 4.0 (Pedersen et al., 1979). These results indicate that an abomasal luminal pH > 3.0 and > 4.0 will be accompanied by a slower activation rate of pepsinogen and prochymosin, respectively, thereby markedly decreasing the proteolytic activity of abomasal secretions. Because abomasal ulcers are most frequently observed in older calves where pepsinogen is the most important proteolytic agent, a general goal of prophylaxis should be to increase abomasal pH to > 3.0 for as long as possible. The results of the study reported here indicate that suckling at 3-h intervals (8x) increases luminal pH > 3.0 for the greatest percentage of the 24-h recording period (Table 1; Figure 6). Mechanical injury to the abomasal mucosa has been considered for many years to be the principle cause of ulceration in calves (Groth and Berner, 1971; Tulleners and Hamilton, 1980; Mei, 1985), as the underdeveloped rumen purportedly allows passage of rough food that has not been adequately ruminated (Gitter and Austwick, 1957). Feeding roughage to veal calves during the fattening period increased the prevalence of abomasal ulceration by 20 to 30% in some studies (Van Putten, 1982; Mei, 1985; Welchman and Baust, 1987) but decreased the prevalence in other studies (Lalles and Toullec, 1998). Although the high prevalence of ulceration in veal calves has been partially attributed to abrasion of the abomasal mucosa in the pyloric antrum, roughage cannot be the critical factor causing ulceration, as the majority of veal calves fed only milk replacer also have ulcers (Wiepkema et al., 1987). Mechanical abrasion is not considered a necessary requirement for the pathogenesis of ulceration in suckling beef calves (Jelinski et al., 1995) because the presence of

FEEDING FREQUENCY AND ABOMASAL PH IN CALVES

trichobezoars in the abomasum does not increase the risk of fatal ulceration (Jelinski et al., 1996). Groth and Berner (1971) reported that, at slaughter, the abomasal luminal pH of veal calves fed straw (3.32) was lower than that of veal calves not fed straw (3.93 [Groth and Berner, 1971]). The results of the study reported here, combined with those of Groth and Berner, suggest that the increased prevalence of abomasal ulceration in veal calves fed straw may be due to a lower luminal pH, rather than the direct effect of mechanical injury to the pyloric antrum. Bacteria and fungi have been frequently isolated from abomasal ulcers (Tulleners and Hamilton, 1980; Lilley et al., 1985; Mills et al., 1990). Clostridium perfringens type A has been isolated from calves with abomasal tympany, abomasitis, and abomasal ulceration (Roeder et al., 1987), and ruminal and abomasal tympany, abomasitis, and abomasal ulceration have been experimentally induced by intraruminal inoculation of C. perfringens type A (Roeder et al., 1988). Fungi have been identified in the abomasal ulcers of suckling calves but are thought to represent a secondary infection after mechanical trauma (Gitter and Austwick, 1957). In general, bacterial and fungal agents are considered postmortem invaders from the alimentary tract or opportunistic secondary infective agents that invade after injury to the abomasal mucosa (Roeder et al., 1988; Welchman and Baust, 1987). A nutritional deficiency of copper has been linked with abomasal ulceration in beef calves in the Western United States (Mills et al., 1990; Lilley et al., 1985); however, these studies did not have an appropriate control group, and definitive evidence of an association between copper deficiency and abomasal ulceration is lacking. Other studies have observed no association between abomasal ulceration and copper deficiency in suckling calves (Roeder et al., 1987, 1988). For many years, stress has also been considered to be involved in the pathogenesis, as ulcers in calves reportedly are found more frequently in calves around the time of weaning (Gitter and Austwick, 1957) or after a period of feed deprivation due to inclement weather (Tulleners and Hamilton, 1980; Lilley et al., 1985). Stress is hypothesized to induce ulcer formation through increased plasma cortisol concentrations, although there is little evidence to support a psychosomatic cause for abomasal ulceration (Welchman and Baust, 1987; Wiepkema et al., 1987). Fasting leads to sustained periods of low pH (Figures 1 and 5; Table 1), and abomasal hyperacidity is probably the major factor promoting ulcer formation. A plausible hypothesis for the development of abomasal ulcers in suckling beef calves is that a sustained period of weather-induced inappetance leads to low abomasal luminal pH, thereby promoting ulcer formation. In ad-

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dition, the presence of poorly ruminated roughage in the abomasum of inappetant beef calves could act to promote ulceration through mechanical damage. Intubation of milk replacer does not induce esophageal groove closure (Chapman et al., 1986). Fluid administered by esophageal intubation initially enters the reticulorumen but flows into the abomasum after administration of 400 ml (Chapman et al., 1986), with the reticulorumen acting as a reservoir of milk replacer. Following intubation, abomasal luminal pH would, therefore, be expected to increase initially to the same extent as when milk replacer is suckled, but would then decrease more rapidly, as observed in this study (Figure 1). The tendency toward sustained higher luminal pH at 8 to 12 h following intubation, compared to suckling, is consistent with the reticulorumen acting as a reservoir of milk replacer. Intubation caused a lower mean 24-h luminal pH than suckling and could, therefore, promote the development of abomasal ulceration. CONCLUSIONS Increasing the frequency of milk replacer suckling increases mean 24-h abomasal luminal pH and percentage of the 24-h period that pH > 3.0 and may, therefore, be efficacious in the prophylaxis of abomasal ulceration in suckling calves. REFERENCES Ahmed, F. A., P. D. Constable, and N. A. Misk. 2002. Effect of an orally administered antacid agent containing aluminum hydroxide and magnesium hydroxide on abomasal luminal pH in clinically normal milk-fed calves. J. Am. Vet. Med. Assoc. 220:74–79. Ahmed, F. A., P. D. Constable, and N. A. Misk. 2001. Effect of orally administered cimetidine and ranitidine on abomasal luminal pH in clinically normal milk-fed calves. Am. J. Vet. Res. 62:1531– 1538. Aukema, J. J., and H. J. Bruekink. 1974. Abomasal ulcer in adult cattle with fatal hemorrhage. Cornell Vet. 64:303–317. Berghen, P., P. Dorny, and J. Vercruysse. 1987. Evaluation of a simplified blood pepsinogen assay. Am. J. Vet. Res. 48:664–669. Breukink, H. J., T. Wensing, J. E. van Dijk, and D. Mevius. 1989. Effect of clenbuterol on the incidence of abomasal ulcers in veal calves. Vet. Rec. 125:109–111. Chapman, H. W., D. G. Butler, and M. Newell. 1986. The route of liquids administered to calves by esophageal feeder. Can. J. Vet. Res. 50:84–87. Dirksen, G. U. 1994. Ulceration, dilatation, and incarceration of the abomasum in calves: Clinical investigations and experiences. Bovine Practitioner 28:127–135. Gitter, M., and P. K. C. Austwick. 1957. The presence of fungi in abomasal ulcers of young calves: A report of seven cases. Vet. Rec. 69:924–928. Glogowski, J. A., and A. G. Rand. 1978. The activation of pepsinogen in extracts of bovine mucosa from the abomasum. J. Dairy Sci. 61(Suppl.1):105. (Abstr.). Groth, W., and H. Berner. 1971. Untersuchungen uber das Labmagengeschwur des Kalbes bei Michaustauschermast und bei Fruhentwohnung. Zbl. Vet. Med. A. 18:481–498. Hafez, E. S. E., and J. A. Lineweaver. 1968. Suckling behavior in natural and artificially fed neonate calves. Z. Tierpsychol. 25:187–198. Journal of Dairy Science Vol. 85, No. 6, 2002

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