Morbidity in Swedish dairy calves from birth to 90 days of age and individual calf-level risk factors for infectious diseases

Preventive Veterinary Medicine 58 (2003) 179–197

Morbidity in Swedish dairy calves from birth to 90 days of age and individual calf-level risk factors for infectious diseases Catarina Svensson a,∗ , Karin Lundborg a , Ulf Emanuelson b , Sven-Ove Olsson c a

Department of Animal Environment and Health, Swedish University of Agricultural Sciences, P.O. Box 234, SE-532 23 Skara, Sweden b Epi-Lys, Funbo Spångtorp, SE-755 97 Uppsala, Sweden c Swedish Dairy Association, P.O. Box 1146, SE-631 804 Eskilstuna, Sweden Received 2 July 2002; accepted 20 January 2003

Abstract The health of 3081 heifer calves born in 122 dairy herds in the south-west of Sweden from 1 January to 31 December, 1998, was monitored from birth until 90 days of age. The calves were kept either in individual pens (n = 2167), in group pens, with 3–8 calves to a pen and manual feeding of milk (n = 440), in group pens with 6–30 calves per pen and an automatic milk-feeding system (n = 431), or with their dams (n = 43). Disease incidence was recorded by farmers and project veterinarians, who clinically examined the calves and auscultated their lungs every 2–3 months. A disease was graded as ‘severe’ if the general loss of condition or of appetite in the calf continued for >2 days or if the animal suffered severe weight loss due to the disease. The effects of season, breed, housing, and type of colostrum feeding, and time, place and supervision of calving on the incidences of diarrhea, severe diarrhea, respiratory disease, other infectious disease and moderately to severely increased respiratory sounds, were analyzed by logistic-regression models (with herd as a random effect). The total morbidity rate was 0.081 cases per calf-month at risk. Incidence rates of arthritis, diarrhea, omphalophlebitis, respiratory disease and ringworm were 0.002, 0.035, 0.005, 0.025 and 0.009 cases per calf-months at risk, respectively. The odds ratios for diarrhea and severe diarrhea were increased in Swedish Red and Whites (OR: 1.6, 2.3) and in calves that received colostrum from first-lactation cows (OR: 1.3–1.8), and for severe diarrhea in calves born in summer or that received colostrum through suckling (OR: 1.7, 1.8). The odds ratios for respiratory disease and increased respiratory sounds were increased in calves housed in large-group pens with an automatic milk-feeding system (OR: 2.2, 2.8). Supervision of calving was associated with a decreased odds ratio for respiratory disease

∗

Corresponding author. Tel.: +46-511-67205; fax: +46-511-67204. E-mail address: [email protected] (C. Svensson). 0167-5877/03/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0167-5877(03)00046-1

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(OR: 0.7) and birth in individual maternity pen or tie stalls with a decreased odds ratio for increased respiratory sounds (OR: 0.5–0.6). Cross-breeds with beef breeds were associated with increased odds ratios for increased respiratory sounds (OR: 2.1–4.3) and colostrum from second-lactation cows and birth during night for other infectious disease (OR: 1.6, 1.5). © 2003 Elsevier Science B.V. All rights reserved. Keywords: Arthritis; Diarrhea; Respiratory disease; Omphalophlebitis; Ringworm; Morbidity; Treatment; Housing; Season; Calves; Colostrum; Calving management

1. Introduction Infectious diseases (especially diarrhea and respiratory illness) are the most important disease problems in young calves (Simensen and Norheim, 1983; Waltner-Toews et al., 1986b; Curtis et al., 1988; Perez et al., 1990; Olsson et al., 1993; Anonymous, 1994; Sivula et al., 1996; Virtala et al., 1996). Presence of diarrhea and/or respiratory illness before 90 days of age affects the performance of the animal later in life and is associated with a higher age at calving (Waltner-Toews et al., 1986a; Correa et al., 1988; Warnick et al., 1994). Warnick et al. (1994) also report that calfhood respiratory disease is associated with an increased occurrence of dystocia at first calving. Britney et al. (1984) found a lower survival in calves that had contracted navel-joint illness before 120 days of age than in healthy calves. Many factors have been associated with an increased risk of infectious disease during the first 90 days of life. Factors that affect the serum immunoglobulin (Ig) concentration are especially important because calves that lack adequate passive immunity have increased mortality rate and are more susceptible to most calfhood infectious diseases than are calves with high Ig concentrations (Blom, 1982; Gay, 1984; Robison et al., 1988; Wittum and Perino, 1995; Donovan et al., 1998; Virtala et al., 1999). The amount of Ig absorbed from the intestine of the calf depends on the amount of ingested colostrum, the Ig concentration of the colostrum, and the absorption efficiency of the gut. Factors which affect these parameters include the age of the calf at first feeding, the method of colostrum feeding, the age (parity) of the dam from which the colostrum originates, and presence of dystocia (Stott et al., 1979a; Devery-Pocius and Larson, 1983; Eigenmann et al., 1983; Petrie, 1984; Michanek and Ventorp, 1989; Besser et al., 1991). In Sweden, calves traditionally have been housed in individual pens. However, the use of group pens has increased during the past decade (Pettersson et al., 2001) and is expected to increase even further although group housing is a risk factor for calf morbidity (Schmoldt et al., 1977; Waltner-Toews et al., 1986b; Perez et al., 1990; Olsson et al., 1993). Previous studies also have reported an increased incidence of respiratory disease during the cold season (Dennis, 1986). Our aim was to describe the incidence and treatment of disease and investigate the effect of breed, type of colostrum feeding, place and supervision of calving, housing and season on the incidence of infectious diseases in 0–90-day-old dairy calves reared under Swedish conditions.

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2. Materials and methods In October 1997, we identified all dairy farms in the former county of Skaraborg, which were enrolled in the official milk-recording program and had 28–94 cows. (For a description of the official Swedish milk-recording program see Andersson (1988).) All these 521 farms (except 36 whose owners were not considered by the large-animal practitioners and agricultural advisors in the region to be capable of keeping reliable records of their calves’ performance) were sent a short questionnaire about housing of replacement heifers, along with a request to include them in this observational study. Three hundred and fifty five (73%) farmers responded the questionnaire and of these 136 farmers expressed willingness to participate in the study. All herds in which young calves were housed in individual or group pens and older calves were kept in group pens with either a slatted floor or straw bedding were included. The study comprised all heifer calves born on these 122 farms during 1998 (a total of 3081 calves). 2.1. Housing, feeding and management Data on housing, feeding, and management of the calves were collected through interviews with the farmers and weighings of concentrates and roughage which were being given, according to the farmers. The housing systems used are shown in Table 1. Calves in individual pens were housed individually until at least 5 weeks old. Group pens for 3–8 calves with manual feeding of the milk were classified as small and those for 6–30 calves with an automatic milk-feeding system were classified as large. Calves in large-group pens were kept individually until 1–2 weeks old. Calves received whole milk until weaning in 45% of the herds (55), milk replacement (55 herds) or a combination of milk replacement and whole milk (12 herds). The milk volumes given ranged from 3 to 8 l per day (median 5.0). The calves were weaned at a median of 9 weeks of age (10–90th percentiles: 8–11 weeks). Except in two herds where calves were fed silage, the calves were given free access to hay as of day 1–25 (median: 1 day; 10–90th percentiles: 1–7 days). Concentrates were given starting from day 1 to 112 (median: 1 week; 10–90th percentiles: 0.5–2.5 weeks). Fifty five herds were fed pelleted calf feed, 47 herds were fed crushed grain (mainly oats and barley) solely or in combination with protein feed, and eight herds were given pelleted cow feed or protein feed alone. In 10 herds, different feedstuffs were used for calves born in spring and calves born in the fall. The concentrates were given ad libitum in 88% of the herds. It was possible to estimate the amount of concentrates fed at 4 weeks of age and at weaning in 71 and 89% of the herds, respectively, and the corresponding percentages for roughage were 55 and 67%. At 4 weeks of age, a median of 0.5 kg of concentrates (10–90th percentiles: 0.3–1.0 kg) and 0.2 kg of hay (10–90th percentiles: 0.05–0.4 kg) were given and at weaning, a median of 1.3 kg concentrates (10–90th percentiles: 0.7–1.75 kg) and 0.8 kg of hay (10–90th percentiles: 0.4–1.7 kg) were given. Data on housing, feeding, and management of young calves were similarly collected for a control group of dairy farms with 28–94 cows from all over Sweden using a self-administered questionnaire. The 1500 farms were selected from all 5800 farms associated with the official milk-recording scheme with 28–94 cows, by means of random numbers. The questionnaire comprised 46 multiple-choice questions and 25 semi-closed questions; of seven sections,

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Disease

Arthritis Diarrhea Omphalophlebitis Ring worm Respiratory disease Weak-calf syndrome Other diseases a

Total (n = 3081)

Individual pen (n = 2167)

Large-group pen (n = 431)

Small-group pen (n = 440)

With cow (n = 43)

Incidence risk

Incidence rate

Incidence risk

Incidence rate

Incidence risk

Incidence rate

Incidence risk

Incidence rate

Incidence risk

Incidence rate

0.6 9.8 1.3 2.5 7.0 1.1 4.4

0.002 0.035 0.005 0.009 0.025 0.004 0.016

0.6 10.0 1.4 2.3 5.4 1.4 3.9

0.002 0.034 0.005 0.008 0.019 0.005 0.013

1.1 9.0 0.9 5.8 14.1 0.2 8.4

0.004 0.031 0.003 0.020 0.048 0.001 0.28

0.5 9.8 1.8 0.7 8.6 0.5 3.2

0.002 0.043 0.008 0.003 0.038 0.002 0.14

0 7.0 0 2.3 0 0 7.0

0 0.025 0 0.008 0 0 0.025

Calves could have more than one disease, but could not have multiple episodes of the same disease.

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Table 1 Incidence risks (%) and rates (cases per calf-month at risk) of the most common diseases in 3081 ≤90-day-old calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999 by type of housinga

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one dealt with young calves. The questionnaire was examined by five veterinarians and one animal scientist before it was mailed, and the questions had been pre-tested by three of the veterinarians during the interviews on the 122 study farms. In total, 877 (58.5%) of the questionnaires were returned (Pettersson et al., 2001). 2.2. Records of diseases and treatment, and presence of calf-level risk factors The farmers were requested to record all cases of disease (both treated and untreated) in the heifer calves on individual health forms. Farmers were to record all therapeutic treatments (pharmaceutical as well as non-pharmaceutical) and note down the person who initiated the treatment (the farmer, a veterinarian, or the farmer after consultation with a veterinarian). For each calf, they also were to record the breed and information about the following potential risk factors for disease: 1. place of birth (i.e., in individual maternity pen, group maternity pen, cubicle, tie stall, the pasture, or another place); 2. time of birth (day1 or night); 3. whether or not the calving was supervised2 ; 4. time of first observed ingestion of colostrum (hours after birth); 5. the main method of feeding the two first meals of colostrum to the calf (bucket/nipple, suckling the dam, or a combination of these); 6. the main source of the first two meals of colostrum fed to the calf (heifer, second calving cow, cow that had calved three or more times). From February 1998 to March 1999, a project veterinarian or research staff visited the farms at least every other month (6–10 times, median 8) to check the records kept by the farmers and complete any missing data. The number of visits per farm by a project veterinarian ranged from 5 to 9 (median 7). During the visits, the veterinarian clinically examined all calves presently born, auscultated their lungs, and recorded prevalent diseases not detected by the farmers in the health records. In total, 2441 (79%) of the calves had one or more lung auscultations. The percentages of animals that were examined among calves housed in individual, large-group or small-group pens, and with the cow were 79, 85, 76, and 58%, respectively. The veterinarian graded the diseases recorded into ‘mild’ or ‘severe’ cases, mainly on the basis of information given by the farmers: calves that had lost condition or their appetite for >2 days or that had suffered obvious weight loss while diseased were categorized as having had a severe disease. Cases that were difficult to grade into one of these categories were denoted as ‘moderate’. Arthritis was defined as swelling of one or more joints accompanied by lameness and fever. Diarrhea was defined as feces with a consistency that was looser than normally observed in calves, continuing for ≥2 days. Omphalophlebitis was defined as a warm swelling or abscess formation associated with the navel. Respiratory disease was defined as coughing or sneezing for >2 days, or severely increased respiratory 1 ‘Day’ was defined as the time of milking and feeding the herd in the morning and evening and the time in between these events. 2 To supervise the calving was defined as checking on the dam at least once every-other hour from recognition of the first signs of closely approaching calving until the birth of the calf.

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sounds at lung auscultation, or moderately increased respiratory sounds together with additional signs (such as coughing or increased nasal discharge). Ringworm was defined as circumscribed crusting patches of alopecia. Weak-calf syndrome was defined as moderately to severely reduced general condition without other disease symptom than (in some cases) fever. Cases of other diseases that were thought to have an infectious origin were categorized as other diseases of presumed infectious origin (not taking into account that some of them may have been of non-infectious origin). Lung-auscultation findings were ranked as normal respiratory sounds or as mildly, moderately or severely increased respiratory sounds. The period from 1 May to 31 August (when the cows and young stock are on pasture, only young calves are kept indoors, the weather is usually dry and the calf premises most often are high-pressure cleaned) was defined as summer; 1 September to 30 November (when cows and young stock return from pasture and the weather is often humid) was defined as fall and 1 December to 30 April (when young stock and cows are kept indoors, calf premises most often have been used by a number of calves since previous high-pressure cleaning and the weather may be cold) as winter. 2.3. Statistical analyses Incidence rates were calculated using calf-months at risk as denominator. Calves that were lost from the study before 90 days old were counted as contributing with the months previous to the loss and half of the month they were lost. The effect of breeds, season, housing, colostral feeding, and time and place of birth on the risk of diseases between day of birth (day 0) and day 90 after birth was evaluated using a generalized linear mixed model with a logit link function. Herd-level variation was accounted for by including a random effect of herd, as applied in the SAS macro GLIMMIX (Littell et al., 1996). Calves housed with the cows were excluded from the analysis because of their low number, leaving a total of 3038 observations. The lung-auscultation findings were categorized as ‘0’ if the respiratory sounds were normal or only mildly increased and ‘1’ if moderately to severely increased. Cases of arthritis, omphalophlebitis, weak-calf syndrome and other diseases of presumed infectious origin were categorized as ‘other infectious disease’. The univariable effect of potential risk factor on the risks of diarrhea, severe diarrhea, pneumonia, other infectious disease and moderately to severely increased respiratory sounds was examined variable by variable, with the herd effect forced into the model. All variables associated (P < 0.20, two-sided) with odds ratios for disease were offered to an initial multivariable model. This model then was reduced using a backward stepwise procedure, with P < 0.10 as the exclusion criterion. Possible interactions between variables in the model were studied with respect to biological relevance, but none was identified as plausible and no interaction terms therefore were fitted in the model. Least-square mean (LSM) equivalents were calculated as k ·β, where k is a vector of weights constructed as for LSMs in the ordinary linear model, and β a vector of solutions for the fixed effects from the generalized linear mixed model. The LSM equivalents on the logit scale were back-transformed by applying the inverse logit link function—thus providing corrected incidence risks. Odds ratios, with 95% confidence limits, were constructed from the final parameter estimates.

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The ages at disease in calves with respiratory disease and diarrhea, respectively, were compared using Wilcoxon’s two-sample test. The hypotheses that group housing of calves is associated with an earlier onset and more severe cases of diarrhea and respiratory disease were examined by the Kruskall–Wallis test. Pair-wise comparisons were made using the Wilcoxon’s two-sample test and P-values were corrected according to Bonferroni. The housing systems and the routines of management and feeding used on the 122 farms were compared with those of the 877 farms that returned the questionnaire; we used the chi-square test, a two-sample t-test, and Mann–Whitney U tests. Confidence intervals (CIs; 95%) for the differences between groups were constructed correspondingly. For these analyses, the software Minitab® Release 10.2 (Minitab, State College, PA, USA) was used. All other analyses were performed using SAS® version 8.1 for Windows (SAS Institute, Cary, NC, USA). P < 0.05 were used to determine statistical significance.

3. Results Ninety two calves died, 16 were slaughtered, 24 were sold, and 2 were lost to the study before 90 days of age, leaving a total of 8722 calf-months at risk. Altogether, 708 (23.0%) of the calves developed one or more diseases between days 0 and 90. Diarrhea occurred most commonly, followed by respiratory disease (Table 1). In addition, 14 (0.5%) calves developed cheek abscesses or actinosis and 23 (0.7%) contracted other diseases of presumed infectious origin. Bloat was diagnosed in 10 (0.3%) and other non-infectious digestive disorders in 21 (0.7%) calves. Malformations were observed in 34 (1.1%) calves, traumatic injury in 18 (0.6%), and deficiency disease in 5 (0.2%) of the animals. Remarks at lung auscultation were recorded in 600 (19.4%) calves, 177 (5.7%) of which were diagnosed with moderately to severely increased respiratory sounds. Most of the 317 cases of diarrhea (68%) were mild, 9% were moderate, and 23% severe. In 60 (19%) of the cases (21 (6.6%) of which were severe), the calves received oral electrolyte solution. In 84 (26%) of the cases, the volume of milk or milk replacement or ration of concentrates was withdrawn or reduced. Ninety five (30%) cases (mainly (61%) moderate to severe ones) were treated with antibiotics (mainly oral). Fifteen cases (5%) had other treatments (mainly homeopathic drugs). Diarrhea was diagnosed at a significantly (P < 0.0001) lower age (median 26 days) than respiratory disease (median of 52 days) (Fig. 1). The 221 cases of respiratory disease included 46% mild, 8% moderate and 46% severe. Approximately half (47%) of the cases (most of which were severe (77%) or moderate (12%)) were treated with parenteral antibiotics. Of the 334 treatments with antibiotics and/or electrolyte solution that were carried out in calves with diarrhea, respiratory disease, or another presumed infectious disease, 72% were initiated by the farmer, 9% by a veterinarian, and 19% by a farmer on the veterinarian’s recommendation. Diarrhea cases were treated by the farmers in 83%, by veterinarians in 2% and by farmers on the veterinarian’s recommendation in 15% of the cases. The median time to feed the first colostrum stated by the farmer was 3.0 h (10–90th percentiles: 1.0–6.5 h). The distributions of the other risk factors included in the analyses are shown in Tables 2–6.

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Fig. 1. Age distribution of diarrhea and respiratory disease in 0–90-day-old dairy calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999.

The odds ratios for diarrhea and severe diarrhea, respectively, were associated with source of colostrum and breed. In addition, the odds ratio of severe diarrhea was associated with season and manner of feeding colostrum (Tables 2 and 3). Cases of diarrhea in calves housed in large-group pens were significantly more severe than those in individually housed calves (P < 0.001) and there was a tendency (P = 0.09) for them to be more severe than was diarrhea in calves housed in small-group pens. Diarrhea was diagnosed at a significantly (P = 0.04) lower age in calves housed in small-group pens (median: 16 days, 10–90th percentiles: 5–72 days) than in those housed in individual pens (median: 30 days, 10–90th percentiles: 7–71 days). The odds ratios for respiratory disease and moderately to severely increased respiratory sounds, respectively, were associated with housing and season (Tables 4 and 5). In addition, the odds ratio for respiratory disease was associated with supervision of calving and the odds ratio for increased respiratory sounds was associated with place of birth and breed. Furthermore, there was a tendency (P = 0.078) for birth during the day to be associated with an increased odds ratio of having increased respiratory sounds. There was no difference in age (P = 0.14) when respiratory disease was diagnosed or in the severity of the cases (P = 0.37) between calves in different housing systems. Risk factors associated with infectious disease other than diarrhea and respiratory disease were source of colostrum and time of birth (Table 6). The highest odds ratio was found in calves that had received colostrum from a second-lactation cow. In contrast to the situation regarding odds ratios for severe diarrhea and increased respiratory sounds, the odds ratio for other infectious disease was higher in calves born during the night.

Variable

Levelsa

No. of animals

Intercept Breed

b

S.E.(b)

OR

95% CI (OR)

−2.41

0.25

–

–

P

Corrected incidence %

95% CI

0.019

6.5 9.9 6.7 4.0

4.9, 8.6 7.7, 13 3.0, 14 1.1, 14

SLB SRB SLB × SRB Cross-breed beef

1515 1418 70 35

0 0.45 0.034 −0.52

– 0.15 0.43 0.69

1.6 1.0 0.60

1.2, 2.1 0.5, 2.4 0.15, 2.3

Housing

Large-group pen Single pen Small-group pen

431 2167 440

0 0.055 0.64

– 0.27 0.32

1 1.7 1.91

– 1.0, 2.9 1.0, 3.5

0.091

4.4 7.4 8.1

2.4, 8.1 4.9, 11 4.9, 13

Season

Winter Fall Summer

1265 871 902

0 0.097 0.30

– 0.15 0.14

1 1.1 1.4

1 0.83, 1.5 1.0, 1.8

0.096

5.7 6.2 7.5

3.6, 8.9 3.9, 9.8 4.8, 12

Source of colostrum

First-lactation cow Second-lactation cow ≥Third-lactation cow

1029 726 1228

0 −0.47 −0.30

– 0.16 0.13

1 0.74 0.63

– 0.57, 0.96 0.46, 0.85

0.0064

8.2 5.3 6.2

5.3, 13 3.2, 8.5 3.9, 9.6

Time of birth

Night Day

1070 1882

0 0.23

– 0.13

1 1.3

– 0.98, 1.6

0.069

7.2 5.8

4.7, 11 3.7, 9.1

C. Svensson et al. / Preventive Veterinary Medicine 58 (2003) 179–197

Table 2 Final logistic-regression model of the incidence risk of diarrhea (and corrected incidence risks) in ≤90-day-old calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999

a SLB: Swedish Holstein; SRB: Swedish Red and White breed; SLB × SRB: all cross-breeds between Swedish Red and Whites and Swedish Holsteins; cross-breed beef: cross-breeds with a dam of Swedish Red and Whites or Swedish Holsteins and a sire of beef breed.

187

188

Variable

Levelsa

No. of animals

b

S.E.(b)

OR

95% CI (OR)

P

Corrected incidence %

95% CI

−4.51

0.32

–

–

Breed

SLB SRB SLB × SRB Cross-breed beef

1515 1418 70 35

0 0.82 1.20 0.55

– 0.25 0.57 0.86

1 2.3 3.2 1.7

– 1.4, 3.7 1.1, 10 0.3, 9.4

0.0059

1.7 3.8 5.5 2.9

1.1, 2.6 2.7, 5.4 1.9, 15 5.6, 14

Colostrum feeding

Nipple/bucket Suckling

1906 1021

0 0.57

– 0.22

1 1.8

– 1.1, 2.7

0.011

2.4 4.2

1.4, 4.2 2.3, 7.5

Season

Winter Fall Summer

1265 871 902

0 0.077 0.55

– 0.25 0.22

1 1.1 1.7

– 0.66, 1.8 1.1, 2.7

0.024

2.6 2.8 4.5

1.4, 4.7 1.5, 5.3 2.5, 7.8

Source of colostrum

First lactation cow Second lactation cow ≥Third lactation cow

1029 726 1228

– 0.24 0.22

1 0.76 0.57

– 0.48, 1.2 0.37, 0.88

0.038

4.2 3.2 2.4

2.4, 7.2 1.7, 6.0 1.3, 4.5

Time to colostrum

Continuous

Intercept

0 −0.28 −0.56 0.066

0.038

0.081

SLB: Swedish Holstein; SRB: Swedish Red and White breed; SLB × SRB: all cross-breeds between Swedish Red and Whites and Swedish Holsteins; cross-breed beef: cross-breeds with a dam of Swedish Red and Whites or Swedish Holsteins and a sire of beef breed. a

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Table 3 Final logistic-regression model of the incidence risk of severe diarrhea (and corrected incidence risks) in ≤90-day-old calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999

Variable

Levels

No. of animals

Intercept

b

S.E.(b)

OR

95% CI (OR)

−3.63

0.21

–

–

P

Corrected incidence %

95% CI

Housing

Single pen Small-group pen Large-group pen

2167 440 431

0 −0.077 0.77

– 0.24 0.28

1 0.93 2.2

– 0.57, 1.5 1.2, 3.8

0.019

3.5 3.3 7.4

2.7, 4.7 2.0, 5.3 4.4, 12

Season

Summer Fall Winter

902 871 1265

0 0.85 0.69

– 0.18 0.18

1 2.3 2.0

– 1.6, 3.4 1.4, 2.8

<0.0001

2.7 6.1 5.2

1.8, 4.0 4.3, 8.5 3.8, 7.1

Supervision of calving

No Yes

1508 1483

0 −0.37

– 0.14

1 0.69

– 0.53, 0.91

0.0083

3.7 5.3

2.6, 5.2 3.9, 7.2

C. Svensson et al. / Preventive Veterinary Medicine 58 (2003) 179–197

Table 4 Final logistic-regression model of the incidence risk of respiratory disease (and corrected incidence risks) in ≤90-day-old calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999

189

190 Table 5 Final logistic-regression model of the incidence risk of moderately to severely increased respiratory sounds (and corrected incidence risks) in ≤90-day-old calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999 Levelsa

No. of animals

b

S.E.(b)

OR

95% CI (OR)

P

Corrected incidence %

Intercept

−2.47

0.59

–

–

95% CI

Birth place

In cubicle or group maternity pen In individual maternity pen In tie stall On the pasture

237 810 1504 487

0 −0.61 −0.55 0.011

– 0.28 0.28 0.29

1 0.54 0.58 1.0

– 0.32, 0.94 0.33, 1.0 0.57, 1.8

0.018

6.2 3.5 3.7 6.3

3.4, 11 2.0, 6.0 2.2, 6.0 3.7, 10

Breed

Cross-breed beef SLB SRB SLB × SRB

35 1515 1418 70

0 −0.75 −1.14 −1.48

– 0.50 0.51 0.73

1 0.47 0.32 0.23

– 0.17, 1.3 0.12, 0.87 0.05, 0.95

0.032

10 5.2 3.6 2.6

4.1, 24 3.7, 7.3 2.5, 5.1 0.85, 7.5

Housing

Single pen Small-group pen Large-group pen

2167 440 431

0 −0.090 1.05

– 0.28 0.29

1 0.91 2.9

– 0.53, 1.6 1.6, 5.0

0.0009

3.5 3.2 9.4

2.2, 5.5 1.7, 5.8 5.2, 16

Season

Summer Fall Winter

902 871 1265

0 0.63 −0.21

– 0.19 0.21

1 1.9 0.81

– 1.3, 2.7 0.54, 1.2

<0.0001

4.2 7.5 3.4

2.5, 6.8 4.7, 12 2.0, 5.6

Time of birth

Night Day

1070 1882

0 0.28

– 0.16

1 1.32

– 0.97, 1.8

0.078

4.2 4.2

2.5, 6.7 2.5, 6.7

a SLB: Swedish Holstein; SRB: Swedish Red and White breed; SLB × SRB: all cross-breeds between Swedish Red and Whites and Swedish Holsteins; cross-breed beef: cross-breeds with a dam of Swedish Red and Whites or Swedish Holsteins and a sire of beef breed.

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Variable

Variable

Levels

No. of animals

b

S.E.(b)

OR

95% CI (OR)

P

Corrected incidence %

95% CI

−3.29

0.18

–

–

Source of colostrum

First lactation cow Second lactation cow ≥Third lactation cow

1029 726 1228

0 0.44 −0.051

– 0.21 0.21

1 1.6 0.95

– 1.0, 2.4 0.63, 1.4

0.033

3.1 4.8 3.0

2.3, 4.3 3.5, 6.5 2.2, 4.0

Time of birth

Night Day

1070 1882

0 −0.39

– 0.17

1 0.68

– 0.48, 0.95

0.022

4.3 2.9

3.2, 5.6 2.3, 3.8

Intercept

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Table 6 Final logistic-regression model of the incidence risk of infectious disease other than diarrhea and respiratory illness (and corrected incidence risks) in ≤90-day-old calves from 122 dairy farms in south-west Sweden in January 1998 to March 1999

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The study farms did not differ significantly from the questionnaire farms with regard to distribution of housing system, type of milk feeders, volume of colostrum, type and number of meals and volumes of milk, type of concentrates, routines for separation of the calf from the cow, criteria for weaning, or replacement percentage. However, they were on average larger than the questionnaire farms (50.7 versus 44.5 cows; 95% CI for difference: 3.2, 9.1), and had a higher average milk production (8762 versus 8544 kg energy-corrected milk; 95% CI for difference: 38, 398). There were also biologically small but statistically significant differences regarding some feeding routines. Calves on the study farms had access to hay (95% CI for difference: 1; 3 days of age) and concentrates somewhat earlier (95% CI for difference: 0.0001; 0.5 weeks) and were weaned somewhat later (95% CI for difference: 0.0001; 0.5 weeks) than were calves on the questionnaire farms.

4. Discussion The total morbidity found in the present study is of a similar level as that previously reported from New York, USA, by Curtis et al. (1988) and from Minnesota, USA, by Sivula et al. (1996). However, it is low in comparison with most reports from other countries, for instance, Blom (1982) reports a similar incidence of enteritis (10.3%) but a considerably higher incidence of respiratory disease (44.0%) in Denmark. Perez et al. (1990) and Wells et al. (1996), by contrast, reported a similar incidence of respiratory disease (5.8–8.4%), but a higher level of diarrhea (24.6%) in dairy calves in The Netherlands and USA, respectively. Waltner-Toews et al. (1986b), Gardner et al. (1990), and Virtala et al. (1996) found higher incidences of both diarrhea (20.5%, 0.12 cases per calf-month at risk, and 28.8%) and respiratory disease (15.4%, 0.077 cases per calf-month at risk, and 25.6%) in calves from Ontario, Canada, and California and New York, USA, respectively. The lower incidence in the present study might be from the low animal density and the small size of farms in Sweden (36 cows per dairy herd associated with the official milk recording program in 1998; Anonymous, 1999) compared with most other countries in western Europe as well as USA. The incidence of diarrhea found in the present study is of a similar level as that reported in previous Swedish studies (Olsson et al., 1993; Viring et al., 1993). Olsson et al. (1993) report an incidence of respiratory disease of 0.8%, which is considerably lower than the 7.0% we found. This difference probably arises from the different methodology used in the two studies. In the work by Olsson and co-workers, farmers made the diagnosis, but we also used study veterinarians. The percentage of the calves treated for pneumonia (3.3%) mainly reflects cases diagnosed by farmers and therefore might be more comparable to the 0.8% reported by Olsson and co-workers (1993). The project veterinarian first diagnosed most of the remaining cases and the relatively high percentage, of 3.7%, of cases that farmers failed to diagnose indicates that pneumonia is difficult to detect. That we used larger herds (28–94 versus 20–50 cows) that were from Skaraborg (the region in Sweden which is most densely populated with cattle)—whereas Olsson et al. studied a sample of dairy herds from all over the country—also might have contributed to the differences in incidences between the two studies. To some extent, the difference may also be due to the increasing use of group pens in Swedish dairy herds.

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A project veterinarian visited the herds between five and nine times during the study period and 79% of the calves had a clinical examination including lung auscultation. More frequent visits most likely would have resulted in more cases of pneumonia being detected; the recorded 0.025 cases per calf-month at risk is probably an underestimation of the true incidence. (More frequent visits were, not possible due to economic realities.) The clinical examinations by the veterinarians are likely to have increased the sensitivity of the study to detect also other chronic diseases (such as omphalophlebitis). However, the duration of diarrhea typically was short (which explains why the visits probably did not importantly increase the sensitivity of the study to detect this disease). Despite attempts to select only herds for which records were complete and thorough, Olsson et al. (1993) had to exclude 34.5% of their study materials due to poor record keeping. Because our study also largely was based on farmer records, we decided to use only herds whose owners had volunteered to participate in the study. Through this approach, we might have attracted farmers who are more interested in their animals and production than are Swedish farmers in general; the selection might have favored well-managed farms. This is also indicated by the higher average milk production among the study farms compared with the randomly selected questionnaire farms. Because the etiology of most calf diseases is multi-factorial and management highly affects their incidence, the disease incidence recorded in the present study therefore might be lower than that among a true random sample of Swedish dairy herds consisting of 28–94 cows. On the other hand, the study farms were on average larger than the questionnaire farms and situated in the area that is most densely populated with cattle—factors that might have contributed to a higher disease incidence. Moreover, the study farms’ routines of feeding, housing, and management did not significantly differ from those of the questionnaire farms. We therefore concluded that the study farms in this study are a reasonably representative sample of Swedish dairy farms with 28–94 cows. Animals with diarrhea quickly become dehydrated; fluid therapy is considered crucial in the supportive management of the diarrheic calf (Phillips, 1985; McGuirk, 1998). However, oral electrolyte solutions were initiated in only 19% of the diarrhea cases. Milk fed during oral rehydration therapy previously was thought to exacerbate the diarrhea by providing substrate to the intestinal flora (resulting in fermentation of undigested nutrients and causing excretion of fluid by means of osmosis). Consequently, withdrawal of milk from calves during their first 2 days of diarrhea used to be recommended. In later studies (Heath et al., 1989; Garthwaite et al., 1994), diarrheic calves were found to have sufficient digestive capacity to assimilate the milk. To reduce loss of body weight in calves with diarrhea, farmers now are advised to keep the calves on milk and give them extra fluids through oral electrolyte solution (Garthwaite et al., 1994; McGuirk, 1996, 1998). However, these new recommendations do not appear to have fully reached farmers; 26% of the cases of diarrhea the calves were subjected to a reduction in (or withdrawal of) the volume of milk or milk replacement or ration of concentrates. Recent Swedish studies detected no association between k99+ Escherichia coli and diarrhea in calves (Viring et al., 1993; De Verdier Klingenberg and Svensson, 1998; De Verdier Klingenberg, 1999). Instead, rotavirus and Cryptosporidium parvum were the most common agents of neonatal diarrhea (Viring et al., 1993; De Verdier Klingenberg and Svensson, 1998; De Verdier Klingenberg, 1999). Those results strongly put into question the use of

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antibiotics in nearly one-third of the diarrhea cases. Of the treatments of fluids or antibiotics given to calves with diarrhea, only 17% were given by veterinarians or following recommendation by a veterinarian. One way of improving the agreement between current recommendations and treatments actually given might be to have veterinarians play a more active role in disease management in calves. The odds ratios for diarrhea or severe diarrhea were 1.6–1.7 when comparing if the calf received colostrum from a first-lactation cow or from an older cow. This is in accordance with findings by Devery-Pocius and Larson (1983), Shearer et al. (1992), and Liberg and Carlsson (1998), who report that first-lactation cows have a lower Ig concentration in their colostrum than do older cows. Calves that received their colostrum through suckling the dam had a significantly higher risk of developing severe diarrhea than did calves that were given their first meal by the farmer. Although the presence of the dam and suckling can increase the amount of Ig absorbed (Fallon, 1979; Stott et al., 1979b; Quigley et al., 1995), calves left with their mothers after birth have a delayed average time to ingestion of their first colostrum and often have failed to ingest adequate volumes of colostrum (Besser et al., 1991; Michanek and Ventorp, 1993; Rajala and Castrén, 1995). In our study, time to first ingestion of colostrum was included in the model; we corrected for it. The results therefore might indicate the difficulties farmers have in successfully recognizing the first ingestion of milk in suckling calves. Ventorp and Michanek (1991) reported that when calves finally found a teat, only one-third of them were successful in getting it into their mouths and a number of these sucked the side of the teat. Farmers might not easily distinguish such behavior from successful suckling and might therefore, wrongly assume that a calf has ingested colostrum. The place of birth is important for the calves’ ability to receive an adequate amount of Ig through suckling. Michanek and Ventorp (1993) reported low serum Ig levels in calves born in group maternity pens, and suggested that this is due mainly to suckling alien cows. Curtis et al. (1988) found calves born in stanchions and loose housing to be more likely to develop diarrhea than calves born in maternity pens. In our study, housing in large-group pens with an automatic milk-feeding system was associated with higher odds ratios for respiratory disease (and moderately to severely increased respiratory sounds) compared to single-pen housing. Similar findings were reported by Maatje et al. (1993) and Plath (1999). Respiratory disease is most often caused by viral infections, which are spread by direct contact and aerosol. Older calves are the source of infection for younger calves (Radostits et al., 1994). In the herds with large-group pens a group of calves could comprise calves from 1 week to 3 months of age. For calves, it is natural behavior to lie close together. It is therefore likely that the increased risk of respiratory disease in calves kept in large-group pens mainly arises from close contact between many calves of different ages. A common nipple in the milk-feeding system, of course, provides an additional source of contact and infection, but might not dramatically increase the spread of infections above the level already given by the group size. From a behavioral aspect, large-group pens with an automatic milk-feeding system have several advantages over single pens with manual feeding of milk. They better meet the calves’ social and motional needs and enable them to drink their milk in a more natural way. In our study, there was a tendency for calves in large-group pens with automatic milk feeders to have a lower incidence of diarrhea. This could represent a true effect—perhaps from those advantages.

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However, it might merely reflect difficulties in detecting diarrhea and identifying which of the calves is diarrheic in a large group compared with a small group. That cases of diarrhea in calves in large-group pens were significantly more severe than those of individually housed calves supports this latter theory. Our study provides additional support for how important the situation and course of events during the calf’s first day of life are to the animal’s subsequent health, and further emphasizes the importance of passive immunization. It also identifies a significant discrepancy between recommended and performed treatments of calves with diarrhea (and thus illustrates the need for more advice to farmers who perform most of the treatments). Respiratory disease is more important in Swedish calves than previous studies have indicated—and housing in large pens with an automatic milk-feeding system might pose a health hazard to calves by increasing the risk of this disease.

Acknowledgements The study was financed by the Swedish Farmers’ Foundation for Research, the Swedish Council for Forestry and Agricultural Research, the Stiftelsen Skaraborgs Nötkreatursförsäkringsbolags Fund, AgroVäst, Växjö Djurskyddsförening, and the Swedish Dairy Association. The authors thank the participating farmers for their interest and support. The assistance of Jonica Östlund, of the Swedish University of Agricultural Sciences (SLU), and Lars Spångberg, Katarina Eriksson, Ingrid Gustavsson, May Johansson, Karin Andersson, Catrin Johansson, and Kjell-Åke Johansson, of Skara Semin ekonomiska förening, in visiting the farms is acknowledged, and of Gunilla Jacobsson (SLU), in data processing. We thank Kerstin Plym Forshell (formerly of Svensk Mjölk, present affiliation; Tine Norske Mejerier) for her support in initiating the project. Finally, thanks go to Per Arnesson and Tauno Turtinen, of Skara Semin ekonomiska förening, for their help with practical arrangements.

References Andersson, L., 1988. Swedish dairy herd health programmes based on routine recording of milk production, fertility data, somatic cell counts and clinical diseases. In: Proceedings of the Sixth International Congress on Animal Hygiene, vol. 1, 14–17 June 1988, Skara, Sweden. pp. 190–194. Anonymous, 1994. Dairy heifer morbidity, mortality and health management focusing on preweaned heifers. United States Department of Agriculture. Besser, T.E., Gay, C.C., Pritchett, L., 1991. Comparison of three methods of feeding colostrum to dairy calves. J. Am. Vet. Med. Assoc. 198, 419–422. Blom, J.Y., 1982. The relationship between serum immunoglobulin values and incidence of respiratory disease and enteritis in calves. Nord. Vet. Med. 34, 276–281. Britney, J.B., Martin, S.W., Stone, J.B., Curtis, R.A., 1984. Analysis of early calfhood health status and subsequent dairy herd survivorship and productivity. Prev. Vet. Med. 3, 45–52. Correa, M.T., Curtis, C.R., Erb, H.N., White, M.E., 1988. Effect of calfhood morbidity on age at first calving in New York Holstein herds. Prev. Vet. Med. 6, 253–262. Curtis, C.R., Erb, H.N., White, M.E., 1988. Descriptive epidemiology of calfhood morbidity and mortality in New York Holstein herds. Prev. Vet. Med. 5, 293–307.

196

C. Svensson et al. / Preventive Veterinary Medicine 58 (2003) 179–197

Dennis, M.J., 1986. The effects of temperature and humidity on some animal diseases—a review. Brit. Vet. J. 142, 472–485. De Verdier Klingenberg, K., 1999. Neonatal calf diarrhoea with special reference to rotavirus infections; significance, epidemiology and aspects of prevention. Acta Uni. Agric. Suec. Veterinar. 54. Doctoral thesis. Swedish University of Agricultural Sciences, pp. 25–26. De Verdier Klingenberg, K., Svensson, L., 1998. Group A rotavirus as a cause of neonatal calf enteritis in Sweden. Acta Vet. Scand. 39, 195–199. Devery-Pocius, J.E., Larson, B.L., 1983. Age and previous lactations as factors in the amount of bovine colostral immunoglobulins. J. Dairy Sci. 66, 221–226. Donovan, G.A., Dohoo, L.R., Montgomery, D.M., Bennet, F.L., 1998. Associations between passive immunity and morbidity and mortality in dairy heifers in Florida, USA. Prev. Vet. Med. 34, 41–46. Eigenmann, U.J.E., Zaremba, W., Luetgebrune, K., Grunert, E., 1983. Colostrum intake and immunoglobulin absorption of normal calves and those born with acidiosis. Berl. Münch. Tierärztl. Wochenschr. 96 (4), 109– 113. Fallon, R.J., 1979. The effect of different methods of feeding colostrum on calf blood serum immunoglobulin levels. Curr. Top. Vet. Med. 4, 507–517. Gardner, I.A., Hird, D.W., Utterback, W.W., Danaye-Elmi, C., Heron, B.R., Christiansen, K.H., Sischo, W.M., 1990. Mortality, morbidity, case-fatality, and culling rates for California dairy cattle as evaluated by the national animal health monitoring system, 1986–87. Prev. Vet. Med. 8, 157–170. Garthwaite, B.D., Drackley, J.K., McCoy, G.C., Jaster, E.H., 1994. Whole milk and oral rehydration solution for calves with diarrhoea of spontaneous origin. J. Dairy Sci. 77, 835–843. Gay, C.C., 1984. The role of colostrum in managing calf health. Proc. Am. Assoc. Bov. Pract. 16, 79–84. Heath, S.E., Naylor, J.M., Guedo, B.L., Petrie, L., Rousseaux, C.G., Radostits, O.M., 1989. The effects of feeding milk to diarrheic calves supplemented with oral electrolytes. Can. J. Vet. Res. 53, 477–485. Liberg, P., Carlsson, J., 1998. Colostrum in Swedish dairy cows: quality and effects on passive immunity in the calves. In: Proceedings of the Xth International Congress on Production and Diseases of Farm Animals, Utrecht, The Netherlands, 24–28 August 1998. p. 98. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., 1996. SAS System for Mixed Models. SAS Institute, Inc., Cary, NC, USA. Maatje, K., Verhoeff, J., Kremer, W.D.J., Cruijsen, A.L.M., Van den Ingh, T.S.G.A.M., 1993. Automated feeding of milk replacer and health control of group-housed veal calves. Vet. Rec. 133, 266–270. McGuirk, S.M., 1996. Neonatal calf management: a guide to disease investigation. In: Proceedings of the World Buiatrics Congress, Edinburgh, vol. 1. pp. 89–92. McGuirk, S.M., 1998. New approach to electrolyte therapy. Cattle practice 6, 67–69. Michanek, P., Ventorp, M., 1989. Intestinal transmission of macromolecules in newborn dairy calves of different ages at first feeding. Res. Vet. Sci. 46, 375–379. Michanek, P., Ventorp, M., 1993. Passive immunization of new-born dairy calves on three farms with different housing systems. Swed. J. Agric. Res. 23, 37–43. Olsson, S.-O., Viring, S., Emanuelson, U., Jacobsson, S.-O., 1993. Calf diseases and mortality in Swedish dairy herds. Acta Vet. Scand. 34, 263–269. Perez, E., Noordhuizen, J.P.T.M., Van Wuijkhuise, L.A., Stassen, E.N., 1990. Management factors related to calf morbidity and mortality rates. Livest. Prod. Sci. 25, 79–93. Petrie, L.M., 1984. Maximising the absorption of colostral immunoglobulins in the newborn dairy calf. Vet. Rec. 114, 157–163. Pettersson, K., Svensson, C., Liberg, P., 2001. Housing, feeding and management of calves and replacement heifers in Swedish dairy herds. Acta Vet. Scand. 42, 465–478. Phillips, R.W., 1985. Fluid therapy for diarrheic calves. What, how, and how much. Vet. Clin. North Am. Food. Anim. Pract. 1, 541–562. Plath, U., 1999. Beurteilung verschiedener Tränketechniken und Betreuungsmassnahmen hinsichtlich ihrer Auswirkungen auf die oralen Aktivitäten, den Gesundheitszustand und die Mastleitung über zwei bis acht Wochen alter Mastkälber in Gruppenhaltung. Dissertation. Institut für Tierhygiene und Tierschutz der Tierärtzlichen Hochschule Hannover. Quigley, J.D., Martin, K.R., Bemis, D.A., Potgieter, L.N.D., Reinemeyer, C.R., Rohrbach, B.W., Dowlen, H.H., Lamar, K.C., 1995. Effects of housing and colostrum feeding on serum immunoglobulins, growth, and fecal scores of Jersey calves. J. Dairy Sci. 78, 893–901.

C. Svensson et al. / Preventive Veterinary Medicine 58 (2003) 179–197

197

Radostits, O.M., Leslie, K.E., Fetrow, J., 1994. Herd Health. Food Animal Production Medicine, vol. 1, second ed., W.B. Saunders Company, Philadelphia, PA. Rajala, P., Castrén, H., 1995. Serum immunoglobulin concentrations and health of dairy calves in two management systems from birth to 12 weeks of age. J. Dairy Sci. 78, 2737–2744. Robison, J.D., Stott, G.H., DeNise, S.K., 1988. Effects of passive immunity on growth and survival in dairy heifers. J. Dairy Sci. 71, 1283–1287. Schmoldt, P., Lemke, P., Bürger, U., Rieck, H., Rotermund, H., 1977. Der Einfluss unterschiedlicher Haltungsformen auf die Kälbergesundheit in der Tränkmilch periode. Mh. Vet. Med. 32, 11–15. Shearer, J., Mohammed, H.O., Brenneman, J.S., Tran, T.Q., 1992. Factors associated with concentrations of immunoglobulins in colostrum at the first milking post-calving. Prev. Vet. Med. 14, 143–154. Simensen, E., Norheim, K., 1983. An epidemiological study of calf health and performance in Norwegian dairy herds. III. Morbidity and performance: literature review, characteristics. Acta Agric. Scand. 33, 57–64. Sivula, N.J., Ames, T.R., Marsh, W.E., Werdin, R.E., 1996. Descriptive epidemiology of morbidity and mortality in Minnesota dairy heifer calves. Prev. Vet. Med. 27, 155–171. Stott, G.H., Marx, D.B., Menefee, B.E., Nightingale, G.T., 1979a. Colostral immunoglobulin transfer in calves. III. Amount of absorption. J. Dairy Sci. 62, 1902–1907. Stott, G.H., Marx, D.B., Menefee, B.E., Nightingale, G.T., 1979b. Colostral immunoglobulin transfer in calves. IV. Effect of suckling. J. Dairy Sci. 62, 1908–1913. Ventorp, M., Michanek, P., 1991. Cow-calf behaviour in relation to first suckling. Res. Vet. Sci. 51, 6–10. Viring, S., Olsson, S.-O., Alenius, S., Emanuelson, U., Jacobsson, S.-O., Larsson, B., Linde, N., Uggla, A., 1993. Studies of enteric pathogens and gamma-globulin levels of neonatal calves in Sweden. Acta Vet. Scand. 34, 263–269. Virtala, A.-M., Mechor, G.D., Gröhn, Y.T., Erb, H.N., 1996. Morbidity from nonrespiratory diseases and mortality in dairy heifers during the first three months of life. JAVMA 208, 2043–2046. Virtala, A.-M., Gröhn, Y.T., Mechor, G.D., Erb, H.N., 1999. The effect of maternally derived immunoglobulin G on the risk of respiratory disease in heifers during the first three months of life. Prev. Vet. Med. 39, 25–37. Waltner-Toews, D., Martin, S.W., Meek, A.H., 1986a. The effect of early calfhood health status on survivorship and age at first calving. Can. J. Vet. Res. 50, 314–317. Waltner-Toews, D., Martin, S.W., Meek, A.H., McMillan, I., 1986b. Dairy calf management, morbidity and mortality in Ontario Holstein herds. I. The data. Prev. Vet. Med. 4, 103–124. Warnick, L.D., Erb, H.N., White, M.E., 1994. The association of calfhood morbidity with first calving age and dystocia in New York Holstein herds. Kenya Vet. 18, 177–179. Wells, S.J., Garber, L.P., Hill, G.W., 1996. Health status of preweaned dairy heifers in the United States. Prev. Vet. Med. 29, 185–199. Wittum, T.E., Perino, L.J., 1995. Passive immune status at postpartum hour 24 and long-term health and performance of calves. Am. J. Vet. Res. 9, 1149–1154.