Calf mortality in Norwegian dairy herds · and weaned heifers, respectively (USDA, 2007). Sim-ensen (1982a) reported a mortality rate of 4.0%, includ-ing stillbirth, during the first

Calf mortality in norwegian dairy herdsS. m. Gulliksen,*†1 K. I. Lie,‡ t. Løken,* and O. Østerås**Department of Production Animal Clinical Sciences, Norwegian School of Veterinary Science, Oslo, Norway†Department of Cattle Health Services, TINE Norwegian Dairies, Ås, Norway‡Department of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science, Oslo, Norway

aBStraCt

The aims of this study were to estimate mortality rates in Norwegian dairy calves and young stock up to 1 yr of age, identify risk factors for calf mortality, and evaluate the etiology of calf mortality based on post-mortem analyses. The material comprised 3 data sets. The first data set included information on 289,038 off-spring in 14,474 dairy herds registered in the Norwegian Dairy Herd Recording System (NDHRS) in 2005. The second included recordings on 5,382 offspring in 125 Norwegian dairy herds participating in a survey on calf health, and the third included results from postmortem analyses of 65 calves from 37 of the survey herds. The calf mortality rate during the first year of life in all herds registered in the NDHRS was 7.8%, including abortion (0.7%) and stillbirth (3.4%). The overall calf mortality rate in liveborn calves in the survey herds was 4.6%. Cows with severe calving difficulties had an odds ratio (OR) of 38.7 of stillbirth compared with cows with no calving difficulties. Twins and triplets showed an increased risk of stillbirth compared with singletons (OR = 4.2 and 46.3, respectively), as did calves born in free stalls compared with tie stalls (OR = 1.9). Re-spiratory disease increased the risk of death in all age groups with hazard ratios (HR) of 6.4, 6.5, 7.4, and 5.6 during the first week of life, 8 to 30 d of age, 31 to 180 d of age, and 181 to 365 d of age, respectively. Diarrhea increased the risk of death among calves younger than 180 d of age, but the influence was only significant during the first week of life and between 8 to 31 d of age (HR = 2.4 and 2.9, respectively). Calves born during the winter were more likely to die during the first week of life than calves born during the summer (OR = 1.2), and were more likely to die during the first month of life than calves born during the autumn (OR = 1.2). Calf mortality rates in all age groups increased with increasing herd size. Calves housed in a group pen

from 2 wk of age were more likely to die during the first month of life than calves housed individually (HR = 1.5). Bronchopneumonia and enteritis were the most frequent postmortem diagnoses, with proportional rates of 27.7 and 15.4%, respectively.Key words: calf, mortality, dairy, risk factor

IntrODuCtIOn

Increased mortality rates are one of several indica-tors of poor welfare resulting in economic losses in cattle production (Martin and Wiggins, 1973). In the Norwegian dairy cow population, which includes ap-proximately 280,000 calvings per year, deaths among calves and young stock cause annual losses up to 100 million Norwegian kroner (>US$15 million) for Norwe-gian dairy farmers (Østerås et al., 2007a).

Mortality rate is defined as the number of animals that die in a designated period divided by the number of animal-time units at risk during that period (Dohoo et al., 2003). According to Heinrichs and Radostitis (2001), calf mortality can be divided into the follow-ing 4 groups according to age at time of death: abor-tions or prenatal deaths (stillborn from 40 to 270 d of gestation), perinatal mortality (stillborn after 270 d of gestation or until 24 h after birth), neonatal mortality (death between 1 and 28 d of age), and older calf mor-tality (death between 1 and 6 mo of age). Calf mortal-ity rates reported from European countries vary from 4% between 1 to 210 d of life (Svensson et al., 2006) to 7% during the first 180 d of life (including stillbirths) (Agerholm et al., 1993). The National Animal Health Monitoring System (NAHMS) in the United States reported an overall abortion percentage of 4.5% during 2006, and mortality rates of 7.8 and 1.8% in unweaned and weaned heifers, respectively (USDA, 2007). Sim-ensen (1982a) reported a mortality rate of 4.0%, includ-ing stillbirth, during the first 30 d of life in Norwegian dairy herds.

Calves are at highest risk of death during the first 4 wk of life (Agerholm et al., 1993). Dystocia has been reported to be the most important cause of perinatal mortality (Chassagne et al., 1999) and pneumonia and diarrhea the most common causes of neonatal death

J. Dairy Sci. 92:2782–2795doi:10.3168/jds.2008-1807© American Dairy Science Association, 2009.

2782

Received October 14, 2008.Accepted February 10, 2009.1 Corresponding author: [email protected]

(Agerholm et al., 1993; Virtala et al., 1996). However, in most cases, the cause of calf mortality is multifacto-rial, often due to a combination of dam factors, various infective agents, and nonoptimal housing and manage-ment. Among the factors reported to influence the risk of calf mortality are herd size, type of housing, person-nel in charge of calf management, colostrum feeding regimen, sex, and time of separation from dam after calving (Simensen, 1982b; Lance et al., 1992).

Cattle production in Norway has changed consider-ably over time, and during the last 10 yr the average herd size in Norway has increased from approximately 14 cow-years to approximately 20 (cow-year = the sum of days from first calving to culling within one year, divided by 365). Changes in cattle production are con-tinuing today; herd size is increasing, there are more cooperative farms with several owners, and starting in 2004, the authorities demanded that all new stalls built are loose-housing or free-stall systems.. These changes could influence the risk of disease and mortality in calves and young stock.

The aims of the present study were to estimate the mortality rate in calves and young stock of up to 1 yr of age in Norwegian dairy herds, to identify risk factors for calf mortality, and to evaluate the etiology of calf death by postmortem analyses.

materIaLS anD metHODS

Herds Registered in the Norwegian Dairy Herd Recording System

Approximately 97% of all Norwegian dairy herds are included in the Norwegian Dairy Herd Recording System (NDHRS). In the current study, information on 309,361 offspring in 15,050 Norwegian dairy herds in 2005 was extracted from this database. The following calves were excluded: born in herds for which herd size was not registered (n = 9,665); born in a herd other than the current herd (n = 10,440); unknown date of birth, but registered in further production (n = 191); registered as being both aborted and stillborn (n = 2); without registration of life status after birth (n = 20); and sold or slaughtered, but dead within 20 d of life (n = 5). Castrated calves were defined as males (n = 661). The final population in this data set included 289,038 offspring in 14,474 Norwegian dairy herds in 2005 (Table 1).

Herds in a Survey on Calf Health

In February 2004, a longitudinal, cross-sectional sur-vey on calf health in Norway was initiated. Dairy herds recorded in the NDHRS as having at least 15 cow-years

were included for further random sampling. In order that all regions of Norway would be represented, 30 districts were selected. A multistage sampling proce-dure was used to select the study herds (Gulliksen et al., 2008). In total, 135 dairy farmers were willing to participate in the project. Each herd participated for 1 yr. The overall survey period lasted from September 1, 2004, through January 31, 2007.

The farmers participating in the survey received a questionnaire comprising 55 closed questions on hous-ing, management, and feeding routines. All questions referred to the situation in the herd during the study year. A total of 127 (94.1%) farmers completed and returned the questionnaire. Two of the herds were ex-cluded from further analysis because of poor recording, and therefore poor data quality. All data were trans-ferred to a separate database by project personnel. The final population included 5,382 offspring in 2005. Data were extracted from the NDHRS (Table 2), and information on housing, feeding, and management in the 125 Norwegian dairy herds was extracted from the questionnaire (Table 3).

Postmortem Examinations

Postmortem examinations of calves in the survey herds were performed according to standard routines. Calves aborted or stillborn were not examined. Feces were sampled for bacteriological and parasitological analyses, and samples of intestines, liver, lung, kidney, and muscle were fixed in 10% neutral buffered formalin for histopathological examination. Additional formalin-fixed organ samples and bacteriological swabs were submitted on indication. Virological, bacteriological, and parasitological analyses were performed at The National Veterinary Institute or The Norwegian School of Veterinary Science. Each case examined was assigned a main diagnosis based on the postmortem macroscopic and histopathological findings, as well as the results of further laboratory analysis.

Health Recordings and Calf Mortality in the NDHRS

In the NDHRS, calf mortality is classified as abortion (stillborn before 260 d of gestation), stillbirth (death after 260 d of gestation or with 24 h after birth), or death between 24 h after birth and registration in the NDHRS, mandatory within 21 d of age, all as binary traits (0/1). Abortions and stillbirths are recorded as a part of the disease history of the dam. Death later in life is recorded as an individual event of the calf.

Information on diseases and preventive treatments for each animal is regularly reported through the Nor-wegian Cattle Health Recording System (NCHRS).

2783CALF MOrTALITY IN NOrwAY

Journal of Dairy Science Vol. 92 No. 6, 2009

A 3-point scale is used to document and describe the occurrence of calving difficulties, as follows: 1 = calv-ing requiring no assistance, 2 = slight calving problems requiring some assistance, and 3 = difficult calving requiring considerable assistance from the owner or a veterinarian. The occurrence of congenital defects is recorded as a binary trait (0/1). The most frequently

reported diseases of the dam from 15 d precalving and 5 d postcalving were extracted from the NDHRS. This included indigestion, laminitis, metritis, prolapse of the vagina or uterus, prolonged gestation period (>296 d of gestation), retained placenta, ketosis, milk fever, and clinical mastitis. In addition, recordings in calves of respiratory disease, diarrhea, and arthritis were ex-


GULLIKSEN ET AL.2784

Table 1. Variables included in the statistical analysis of possible risk factors for abortion, stillbirth, and death during the first year of life in 289,038 calves in 14,474 dairy herds registered in the Norwegian Dairy Herd Recording System (NDHRS) during 2005

Variable Class Calves (n) Aborted (%) Stillborn (%)

Dead (%)

<8 d8−30 d of age

31–180 d of age

181–365 d of age

Total 289,038 0.74 3.41 0.87 0.67 1.72 0.43Region of Norway Oslo area 11,665 0.74 4.09 1.10 0.64 1.85 0.26

Southeastern 60,482 0.62 3.16 0.75 0.64 1.69 0.41Southern 14,418 0.80 3.45 0.83 0.62 1.73 0.49Western 45,990 1.03 3.74 1.03 0.68 1.87 0.48Northwestern 35,807 0.70 2.67 0.89 0.55 1.40 0.56Mid 91,565 0.65 3.52 0.88 0.76 1.82 0.37Northern 29,111 0.82 3.72 0.79 0.69 1.60 0.46

Herd size (cow-years) ≤5 797 0.75 4.05 1.05 0.13 1.47 0.415.1–10 21,712 0.68 2.84 0.86 0.46 1.32 0.4810.1–15 67,607 0.68 3.04 0.76 0.50 1.43 0.4215.1–20 80,072 0.72 3.36 0.76 0.62 1.60 0.4320.1–30 73,076 0.81 3.47 0.92 0.69 1.85 0.4130.1–50 33,677 0.73 3.97 1.02 0.96 2.12 0.43>50.1 12,097 0.84 4.91 1.58 1.51 3.09 0.57

Breed 1: Norwegian Red (NR) 270,925 0.74 3.33 0.85 0.67 1.72 0.432: Crossbreed with NR 12,784 0.66 4.57 1.27 0.76 1.88 0.443: Other 5,329 0.68 5.06 1.21 0.83 1.32 0.68

Parity 1 108,042 0.58 4.38 1.10 0.65 1.81 0.462 74,390 0.87 2.61 0.73 0.58 1.69 0.433 48,902 0.82 2.73 0.71 0.58 1.71 0.43>3 57,704 0.78 3.22 0.76 0.78 1.62 0.38

Sex of calf Male 148,699 0.07 3.88 1.00 0.73 1.79 0.34Female 137,884 0.05 2.56 0.73 0.62 1.65 0.53Sex unknown 2,455 80.04 100.00 — — — —

Calving season Winter 58,346 0.75 3.72 0.95 0.91 1.83 0.46Spring 67,428 0.73 3.78 0.98 0.77 1.94 0.45Summer 71,454 1.00 3.53 0.83 0.56 1.63 0.35Autumn 91,810 0.53 2.86 0.77 0.55 1.56 0.46

Weekday of calving 1: Weekend 84,233 0.70 3.46 0.87 0.66 1.69 0.432: Week day 204,805 0.75 3.40 0.87 0.68 1.73 0.43

Calves per calving Singletons 274,675 0.00 3.00 0.84 0.67 1.71 0.43Twins 12,175 0.07 12.55 1.54 0.86 1.98 0.58Triplets 67 0.00 43.28 7.89 0.00 2.86 0.00Missing 2,121 100.00 — — — — —

Congenital defects Yes 740 1.08 32.79 27.24 5.87 5.04 1.88No 279,596 0.76 2.32 0.64 0.65 1.71 0.43Unknown 8,702 0.00 35.82 9.97 1.43 2.24 0.33

Calving difficulties None 262,999 0.50 1.77 0.63 0.64 1.67 0.44Moderate 13,646 0.72 11.21 2.00 0.97 2.16 0.34Severe 6,050 1.67 43.08 10.87 1.72 3.20 0.66Unknown 6,343 9.92 18.73 3.90 1.12 2.27 0.37

Purchased dam No 248,951 0.74 3.34 0.86 0.65 1.66 0.42Yes 40,087 0.69 3.86 0.96 0.81 2.11 0.50

Diarrhea No 287,612 — — 0.87 0.66 1.68 0.43Yes 1,426 — — 0.49 3.38 10.36 1.30

Respiratory disease No 287,584 — — 0.87 0.67 1.67 0.42Yes 1,454 — — 0.69 2.29 11.76 3.21

Arthritis No 288,037 — — 0.88 0.66 1.68 0.43Yes 1,001 — — 0.00 4.30 14.41 1.71

tracted from the NDHRS. Further details regarding the health recording system are described by Østerås et al. (2007b).

Statistical Analysis

NDHRS Herds. Data were stored in a central database managed by TINE Norwegian Dairies and

transferred to SAS version 9.1 (SAS Institute Inc., Cary, NC) for descriptive statistics and statistical analyses. Separate multivariable models were fit with abortion, stillbirth, and death from 1 to 7 d of age, 8 to 30 d of age, 31 to 180 d of age, and 181 to 365 d of age as dependent variables, all as binary traits (0/1). PROC GENMOD with binomial distribution and logit link function with Wald’s statistics for type 3 contrasts



Table 2. Variables included in the statistical analysis of possible risk factors for abortion, stillbirth, and death during the first year of life in 5,382 calves in 125 Norwegian dairy herds participating in a survey on calf health during 2005

Variable Class Calves (n) Aborted (%) Stillborn (%)

Dead (%)

<8 d8−30 d of age

31–180 d of age

181–365 d of age

Total 5,382 0.87 3.92 0.74 1.07 2.22 0.63Region of Norway Oslo area 560 2.14 4.01 1.91 0.00 1.75 0.00

Southeastern 1,559 0.83 3.10 0.60 1.35 3.04 0.94Southern 396 1.52 4.10 0.00 0.86 1.80 1.17Western 581 1.03 4.87 0.74 1.48 1.89 0.23Northwestern 588 0.51 3.42 0.53 1.45 1.93 0.53Mid 1,121 0.45 4.12 0.94 0.95 1.15 0.22Northern 577 0.35 5.04 0.37 0.94 3.46 1.44

Herd size (cow-years) ≤5 — — — — — — —5.1–10 — — — — — — —10.1–15 56 1.79 1.82 0.00 1.85 1.92 2.4415.1–20 558 0.54 3.24 0.74 0.38 1.98 0.0020.1–30 1,189 0.76 2.88 0.35 0.45 1.88 0.5130.1–50 1,832 1.04 4.19 0.70 1.23 1.75 0.81>50.1 1,747 0.86 4.62 1.09 1.55 3.05 0.66

Breed 1: Norwegian Red (NR) 5,153 0.89 3.90 0.70 1.12 2.32 0.672: Crossbreed with NR 159 0.63 3.80 1.97 0.00 0.00 0.003: Other 70 0.00 5.71 1.52 0.00 0.00 0.00

Parity 1 2,028 0.89 5.27 1.00 1.40 2.38 0.592 1,324 1.28 2.68 0.47 0.40 1.97 0.583 904 0.55 3.00 0.81 1.17 2.66 0.58>3 1,126 0.62 3.66 0.56 1.23 1.86 0.81

Sex of calf Male 2,764 0.04 4.34 0.91 1.25 2.46 0.79Female 2,556 0.00 2.86 0.57 0.90 1.98 0.52Sex unknown 62 74.19 100.0 — — — —

Calving season Winter 1,242 0.89 5.04 0.94 1.13 1.97 0.63Spring 1,238 0.73 3.99 0.94 1.48 2.35 0.75Summer 1,311 1.07 3.47 0.40 0.90 2.26 0.61Autumn 1,591 0.82 3.36 0.72 0.87 2.27 0.57

Weekday of calving 1: Weekend 1,521 0.85 4.31 0.69 0.99 2.33 0.792: Week day 3,861 0.88 3.76 0.76 1.11 2.17 0.57

Calves per calving Singletons 5,074 0.00 3.35 0.70 1.06 2.14 0.59Twins 261 0.00 14.94 1.82 1.40 3.86 1.78Triplets — — — — — — —Missing 47 100.0 — — — — —

Congenital defects Yes 14 0.00 14.29 20.00 12.50 14.29 0.00No 5,152 0.91 2.64 0.54 0.90 2.17 0.63Unknown 216 0.00 33.33 6.47 6.92 3.31 0.94

Calving difficulties None 4,927 0.53 1.96 0.46 1.02 2.16 0.65Moderate 225 0.89 13.00 3.14 0.54 2.87 0.72Severe 117 2.56 57.02 16.33 0.00 5.00 0.00Unknown 113 14.16 19.59 2.60 6.67 2.86 0.00

Purchased dam No 4,552 0.94 3.84 0.79 1.15 2.12 0.61Yes 830 0.48 4.36 0.51 0.64 2.76 0.74

Diarrhea No 5,220 — — 0.77 0.99 2.06 0.63Yes 162 — — 0.00 3.70 7.24 0.84

Respiratory disease No 5,244 — — 0.77 0.96 1.92 0.60Yes 138 — — 0.00 5.07 13.08 2.02

Arthritis No 5,346 — — 0.75 0.98 2.09 0.64Yes 36 — — 0.00 13.89 22.58 0.00

(Dohoo et al., 2003) was used with herd as random effect. By applying alternative logistic regression, the random effects were expressed as log (odds ratio) by using the LOGOR statement (Carey et al., 1993). Two different models were fit in case of death in the different age groups, except abortion. The first model included all offspring in 2005, whereas the second included off-spring defined as normal; that is, a singleton calf born without congenital defects or calving difficulties. The potential risk factors included in the statistical analysis are presented in Tables 1 and 2. In addition, prolonged gestation period, occurrence of disease in the dam from 15 d before and 5 d after calving, and the occurrence of respiratory disease, diarrhea, or arthritis in the calf were included as fixed effects. A season variable was created for each calf based on the date of birth. Spring, summer, autumn, and winter were defined as March through May, June through August, September through November, and December through February, respective-ly. Hierarchical dummy variables were created for herd size in cow-years, divided into >5, >10, >15, >20, >30, and >50 cow-years. The significance of the different variables was initially evaluated by univariate analysis.

If the P-value was <0.1 the variable was included in a final multivariable model. The overall significance of each variable was evaluated by using manual forward stepwise selection with inclusion criteria of P < 0. 05. Possible interactions between significant fixed effects were tested. The model fit was evaluated by deviance residuals (Dohoo et al., 2003).

Survey Herds. Data were stored in MS SQL Server (Microsoft, Redmond, WA) or a central database man-aged by TINE Norwegian Dairies and transferred to SAS version 9.1 (SAS Institute Inc.) for descriptive statistics and statistical analyses. In the analysis of risk factors for abortion and stillbirth, PROC GENMOD with bi-nomial distribution and logit link function with Wald’s statistics for type 3 contrasts (Dohoo et al., 2003) was used with herd as random effect. Separate multivari-able models were fit, with abortion (0/1) and stillbirth (0/1) as dependent variables. By applying alternative logistic regression, the random effects were expressed as log (odds ratio) by using the LOGOR statement (Carey et al., 1993). In cases of death during the first year of life, survival analysis was performed in the following groups: death from 1 to 7 d, 8 to 30 d, 31 to 180 d, and



Table 3. Variables on housing and management extracted from a questionnaire from 125 dairy herds participating in a survey on calf health in Norway between 2004 and 2007

Variable ClassHerds (N)

Calves (n)

Total 125 5,382Stall type Tie stall 71 2,317

Free stall 54 3,065Born in herd that purchased calves during the last year No 95 3,970

Yes 25 1,187Missing 5 225

Calving facilities Tie stall: in box 71 2,317Free stall: cubicle section or alley area 19 1,023Free stall: calving pen 34 2,006Missing 1 36

Separation from dam Immediately 87 3,465During the first 24 h 27 1,445Later 10 436Missing 1 36

Suckling as feeding regimen No 112 4,756Yes 13 626

First feeding of colostrum after birth Within 30 min 35 1,197Within 2 h 51 2,325Within 4 h 12 542Later 25 1,176Missing 2 142

Minimum colostrum fed first feeding ≤1 L 22 1,0341.1 to 2 L 81 3,226>2 L 14 697Missing 8 425

Confinement from 2 wk of age Single pen 60 2,468Group pen 64 2,893Missing 1 21

Maximum age difference between youngest and oldest calf housed in the same pen <4 wk 50 2,4574 to 8 wk 39 1,703>8 wk 25 817Missing 11 405

181 to 365 d of age. Separate Cox proportional hazard models (Cox, 1972) were fitted by using the PROC PHREG statement with death (0/1) as dependent vari-able, including the positive stable frailty models in the SAS macro available from Shu and Klein (1999, 2005). The significance of the frailty effect was assessed by the likelihood ratio test of independence [H0: Theta (θ) = 1]. The frailty effect equals the strength of association between 2 individuals within the same herd, measured by Kendall’s τ (1 − θ) and was considered significant at P < 0.05. The end of the observation period in a calf was defined as 365 d of age, if death had not occurred. Data were censored when the animal left the herd due to sale or slaughter. To include all calves born in 2005, the observation period in the survey was defined as January 1, 2005, to December 31, 2006. As with the analyses performed on offspring in the NDHRS herds, 2 different models were fit in case of death in all age groups except abortion. The first model included all calvings in 2005, and the second only included calv-ings defined as normal. In addition to the fixed effects included in the analysis of calf mortality in all NDHRS herds (Table 1), variables on housing, feeding, and man-agement were extracted from the survey questionnaire and included (Table 3). Nonsignificant variables were removed one by one by backward stepwise elimination, with an inclusion criterion of P < 0.05. Possible inter-actions between significant fixed effects were tested.

reSuLtS

NDHRS Herds

The mortality rate during the first year of life was found to be 7.8%, including abortion (0.7%) and still-

birth (3.4%). The mortality rates in the different age groups are presented in Table 1.

The factors that had a significant effect on the sur-vival of offspring in the NDHRS herds are presented in Tables 4 to 9.

Cows recorded with slight calving difficulties had an odds ratio (OR) of 7.3 [95% confidence interval (CI): 6.7–7.9] of stillbirth compared with cows recorded as having no calving difficulties. Cows recorded with se-vere calving difficulties had a further increased risk of stillbirth, OR = 5.3 (95% CI: 4.8–5.9), compared with cows registered with slight calving difficulties. Calves recorded with congenital defects were found to have an OR of 10.4 (95% CI: 8.0–13.4) of stillbirth compared with calves born without defects. Twins and triplets had a higher risk of stillbirth than singletons: OR = 4.2 (95% CI: 3.8–4.6) and OR = 46.3 (95% CI: 20.5–104.8), respectively. Factors influencing the risk of stillbirth in normal calvings are presented in Table 5.

Dystocia, congenital defects, and being born as a twin or a triplet were also found to increase the risk of death, during both the first week and the first month of life. Severe calving difficulties increased the risk of death, OR = 4.6 (95% CI: 4.1–5.1) and OR = 1.9 (95% CI: 1.6–2.2), during the first week and first month, re-spectively, compared with normal calvings. Twins and triplets had an increased risk of death during the first week [OR = 1.3 (95% CI: 1.2–1.5) and OR = 4.9 (95% CI: 1.8–13.6), respectively], compared with singletons, but once the calves were older than 1 wk, there was no significant effect on the risk of death for calves born as twins or triplets compared with calves born as single-tons. Calves born with malformations had an increased risk (OR) of death during the first week and first month of life of 16.9 (13.8–20.9) and 5.1 (3.7–7.1), respectively,



Table 4. Factors with a significant effect on risk of abortion in 289,038 pregnancies in 14,474 Norwegian dairy herds during 2005

Fixed effect Class Calves (n) Estimate (β) SE OR (95% CI)1 P-value

Intercept 289,038 −5.13 0.081 <0.001Calving season Winter 58,346 0.32 0.076 1.37 (1.18–1.60) <0.001

Spring 67,428 0.27 0.078 1.31 (1.13–1.52) <0.001Summer 71,454 0.62 0.070 1.85 (1.61–2.12) <0.001Autumn 91,810 0 1.0 —

Parity 1 108,042 0 1.0 —2 74,390 0.39 0.061 1.47 (1.31–1.66) <0.0013 48,902 0.34 0.069 1.40 (1.23–1.61) <0.001>3 57,704 0.30 0.068 1.35 (1.18–1.54) <0.001

Region of Norway Oslo area 11,665 −0.34 0.135 0.71 (0.55–0.93) 0.012Southeastern 60,482 −0.49 0.078 0.61 (0.53–0.72) <0.001Southern 14,418 −0.25 0.121 0.78 (0.62–0.99) <0.05Western 45,990 0 1.0Northwestern 35,807 −0.31 0.095 0.73 (0.61–0.88) 0.001Mid 91,565 −0.46 0.070 0.63 (0.55–0.73) <0.001Northern 29,111 −0.21 0.091 0.81 (0.68–0.97) <0.05

Herd effect (α) 14,474 0.89 0.055 2.43 (2.19–2.71) <0.001

1Odds ratio and 95% confidence interval.

compared with normal calves. The factors influencing the risk of death in calves born from normal calvings from 1 to 365 d of age are presented in Tables 6 to 9. No associations between occurrence of disease in the dam and calf mortality were found in any age group.

Survey Herds

The overall calf mortality rate during the first year of life was found to be 9.5%, including abortion (0.9%) and stillbirth (3.9%). By organizing the herds in de-scending order by mortality rate, the mortality rate in

each herd is presented in Figure 1. The mortality rates in the different age groups are presented in Table 2.

Cows with slight calving difficulties were found to have a greater risk of stillbirth than cows registered with no calving difficulties [OR = 5.1 (95% CI: 2.8–9.2)]. The corresponding increase in stillbirth risk for cows registered with severe calving difficulties was OR = 41.3 (95% CI: 20.2–84.2). Calves born as twins had an increased risk of stillbirth of OR = 3.5 (95% CI: 2.0–6.0) compared with singletons. Respiratory disease was found to increase the risk of death in all age groups (Figure 2) with hazard ratios (HR) of 6.39, 6.49, 7.40,



Table 5. Factors with a significant effect on risk of stillbirth in 246,156 dairy calves1 born in 14,423 Norwegian dairy herds during 2005


Intercept 246,156 −4.93 0.06 <0.001Calving season Winter 49,354 0.18 0.070 1.20 (1.05–1.38) <0.05

Spring 55,908 0.17 0.069 1.19 (1.04–1.36) <0.05Summer 60,484 0.05 0.068 1.06 (0.93–1.21) NSAutumn 80,410 0 1.0 —

Parity 1 90,492 0 1.0 —2 64,817 −0.37 0.063 0.69 (0.61–0.78) <0.0013 42,145 −0.36 0.071 0.70 (0.61–0.80) <0.001>3 48,702 −0.39 0.070 0.68 (0.59–0.78) <0.001

Breed Norwegian Red (NR) 231,105 0 1.0 —Crossbreed with NR 10,562 0.23 0.103 1.26 (1.03–1.55) <0.05Other breed 4,489 0.50 0.153 1.64 (1.22–2.22) 0.001

Herd size (cow-years) ≤20 145,672 0 1.0 —>20 100,484 0.18 0.053 1.20 (1.08–1.33) <0.001

Born from purchased dam Yes 34,131 0.22 0.071 1.24 (1.08–1.43) <0.05No 212,025 0 1.0 —

Herd effect (α) 14,423 0.75 0.080 2.13 (1.82–2.49) <0.001

1Singletons born without congenital defects or calving difficulties.2Odds ratio and 95% confidence interval.

Table 6. Risk factors with a significant effect on mortality during the first week of life in 243,607 dairy calves1 in 14,423 Norwegian dairy herds during 2005


Intercept 243,607 −3.57 0.030 — <0.001Parity 1 89,356 0 1.0

2 64,254 −0.11 0.030 0.90 (0.85–0.95) <0.0013 41,747 −0.14 0.035 0.89 (0.81–0.93) <0.001>3 48,250 −0.19 0.034 0.83 (0.78–0.89) <0.001

Herd size (cow-years) ≤20 144,292 0 1.0 —>20 99,315 0.25 0.033 1.28 (1.2–1.37) <0.001

Calving season Winter 48,802 0.16 0.036 1.17 (1.09–1.25) <0.001Spring 55,287 0.14 0.037 1.15 (1.07–1.24) <0.001Summer 59,870 −0.04 0.036 0.96 (0.90–1.03) NSAutumn 79,648 0 1.0 —

Diarrhea No 242,415 0 1.0Yes 1,192 1.61 0.090 5.00 (4.16–6.0) <0.001

Arthritis No 242,757 0 1.0Yes 850 1.98 0.092 7.30 (6.07–8.70) <0.001

Respiratory disease No 242,387 0 1.0Yes 1,220 1.60 0.103 4.97 (4.06–6.09) <0.001

Herd effect (α) 14,423 0.87 0.089 2.39 (2.00–2.85) <0.001


and 5.59 during the first week, 8 to 30 d, 31 to 180 d, and 181 to 365 d of age respectively. Respiratory disease was the only significant factor influencing the risk of death in calves older than 180 d of age. Diar-rhea increased the risk of death among calves in all age groups younger than 180 d of age (Figure 3), but the influence was only significant during the first week and from 8 to 31 d of age, with HR of 2.38 and 2.94, respectively. Calves registered with arthritis were found to have an increased risk of death during the first 180

d of age with HR varying from 11 to 14, but only 36 (0.67%) of the 5,382 calves were recorded with arthritis during 2005.

Calves born in a free stall were at increased risk of stillbirth compared with calves born in a tie stall [OR = 1.90 (95% CI: 0.95–3.70], although this was only borderline significant (P = 0.06). Suckling calves had an increased risk of death during the first week of life compared with calves fed manually (HR = 1.79, 95% CI: 0.94–1.22, P = 0.07). Calves housed in a group pen



Table 7. Risk factors with a significant effect on mortality from 8 to 30 d of life in 241,329 dairy calves1 in 14,419 Norwegian dairy herds during 2005


Intercept 241,329 −3.70 0.043 — <0.001Parity 1 88,497 0 1.0 —

2 63,675 −0.08 0.032 0.92 (0.87–0.98) <0.053 41,368 −0.10 0.037 0.90 (0.84–0.97) <0.05>3 47,789 −0.16 0.036 0.85 (0.79–0.92) <0.001

Herd size (cow-years) ≤5 632 −0.19 0.296 0.83 (0.46–1.47) NS5.1–10 18,268 −0.16 0.065 0.85 (0.74–0.96) <0.0510.1–15 57,070 −0.12 0.047 0.88 (0.80–0.97) <0.0515.1–20 67,075 0 1.0 —20.1–30 60,677 0.09 0.048 1.10 (1.00–1.20) NS30.1–50 27,745 0.23 0.059 1.26 (1.12–1.42) <0.001>50 9,862 0.59 0.116 1.81 (1.44–2.27) <0.001

Calving season Winter 48,337 0.18 0.041 1.20 (1.11–1.30) <0.001Spring 54,629 0.15 0.042 1.16 (1.07–1.26) <0.001Summer 78,999 0 1.0 —Autumn 59,364 0.04 0.038 1.04 (0.97–1.12) NS

Diarrhea No 240,141 0 1.0 —Yes 1,188 1.73 0.094 5.65 (4.70–6.80) <0.001

Arthritis No 240,479 0 1.0 —Yes 850 2.14 0.090 8.52 (7.13–10.2) <0.001

Respiratory disease No 240,115 0 1.0 —Yes 1,214 1.70 0.103 5.49 (4.49–6.73) <0.001

Herd effect (α) 14,419 0.92 0.08 2.50 (2.12–2.99) <0.001


Table 8. Risk factors with a significant effect on mortality from 30 to 180 d of life in 235,584 calves1 in 14,399 Norwegian dairy herds during 2005


Intercept 235,584 −3.92 0.034 — <0.001Respiratory disease No 234,394 0 1.0

Yes 1,190 1.83 0.105 6.21 (5.05–7.63) <0.001Arthritis No 234,769 0 1.0

Yes 815 2.18 0.103 8.83 (7.22–10.80) <0.001Diarrhea No 234,440 0 1.0

Yes 1,144 1.72 0.103 5.58 (4.56–6.83) <0.001Herd size (cow-years) ≤5 609 −0.01 0.31 0.99 (0.54–1.82) NS

5.1–10 17,680 −0.11 0.071 0.89 (0.78–1.03) NS10.1–15 55,684 −0.10 0.051 0.90 (0.82–1.00) NS15.1–20 59,410 0 1.020.1–30 65,552 0.08 0.052 1.08 (0.97–1.20) NS30.1–50 27,127 0.16 0.064 1.17 (1.04–1.33) <0.05>50 9,522 0.47 0.138 1.60 (1.22–2.09) <0.001

Herd effect (α) 14,399 1.00 0.12 2.73 (2.15–3.47) <0.001


from 2 wk of age were found to have a greater risk of death during the first month of life (HR = 1.5, 95% CI: 0.98–2.27, P = 0.06) than calves housed in a single pen.

Significant cluster effects on herd level were found in all age groups <180 d, with frailty effects varying from 5.0 to 7.2%.

Postmortem results of 65 calves from 37 herds rep-resented 25.9% (65/251) of all calves that died during this period. Of these, 55 (84.6%) examinations were performed by veterinarians in the field, and the other 10 (15.4%) were performed at the National Veterinary Institute or the Norwegian School of Veterinary Sci-ence. Bronchopneumonia was the main diagnosis in 18 (27.7%) of the 65 calves (Table 10). In animals older than 1 mo, bronchopneumonia was the main diagno-sis in 17 (41.5%) of the 41 cases. Bronchopneumonic

changes (gross or histological changes) from very mild to severe lesions were detected in 36 (55.0%) calves. Enteritis was the second most common finding and was considered the main or primary diagnosis in 10 (15.4%) of 65 calves and in 5 (20.8%) of 24 calves who died at less than 1 mo of age.

DISCuSSIOn

Statistical Analysis

Both logistic regression and survival analyses were performed on the data from the total NDHRS popula-tion, and there were no significant differences in the re-sults obtained by the 2 methods. Because of the massive numbers of observations, logistic regression was chosen, as this was the most efficient way to account for the



Table 9. Risk factors with a significant effect on mortality from 180 to 365 d of life in 195,363 calves1 in 14,102 Norwegian dairy herds during 2005


Total 195,363 −5.45 0.071 <0.001Respiratory disease No 194,401 0 1.0

Yes 962 2.01 0.177 7.50 (5.31–10.61) <0.001Calving season Winter 39,600 0.26 0.098 1.29 (1.06–1.57) <0.05

Spring 45,208 0.18 0.102 1.20 (0.98–1.46) NSSummer 62,596 0 1.0 —Autumn 47,959 0.27 0.087 1.31 (1.12–1.56) <0.05

Herd effect (α) 14,102 1.28 0.154 3.59 (2.65–4.85) <0.001


Figure 1. Calf mortality rates (%), including abortion and stillbirth, in 125 Norwegian dairy herds participating in a survey on calf health in 2005. The herds are organized in descending order by mortality rate.

expected cluster effect on herd level. In the less time-consuming analyses that included only survey herds, the cluster effect on herd level was assessed through the frailty effect. Survival analysis was chosen for these data because of the possibility of accounting for calves leaving the herd for reasons other than death, such as sale or slaughter. This was accomplished through right censoring.

Mortality Rate

The mortality rate estimated for the herds registered in the NDHRS was similar to mortality rates reported from other European countries (Olsson et al., 1993; Esslemont and Kossaibati, 1996), lower than that re-ported in the United States (USDA, 2007), but slightly higher than that previously reported from Norway (Si-mensen, 1982a). A lack of a standardized definition of calf mortality means that inter-study comparisons are difficult. Results from the NAHMS in 2006 indicate an abortion rate of 4.5% (USDA, 2007), which is substan-tially higher than the abortion rate of 0.74% reported from the NDHRS (Table 1). This might be partly due to the considerably smaller herds in Norway, and the fact that Norway is free from several important infec-tious diseases of cattle such as brucellosis, leptospirosis, infectious bovine rhinotracheitis, and bovine virus diar-rhea. Svensson et al. (2006) reported a mortality rate of 3% in Swedish dairy calves before 90 d of age, which is

similar to the 3.1% for the same age group in the herds registered in the NDHRS. It might be anticipated that calf mortality rates in these 2 countries would be com-parable because of similar infectious status, although the average dairy herd size in Sweden is slightly larger (Pettersson et al., 2001).

The mortality rate in the survey herds was higher than that of the herds registered in the NDHRS. Mor-tality rate increased in all age groups with increasing herd size, which could be due in part to the larger size of the survey herds [average size of survey herds is 46.8 (SD 27.6) cow-years; average size of herds registered in the NDHRS is 21.6 (SD 13.4) cow-years]. The mortality rates in the 3 largest herd-size groups were similar in NDHRS herds and survey herds, demonstrating that the survey herds could be considered as representative of large Norwegian dairy herds. Abortion and stillbirth are recorded as a part of the disease history of the dam. Hence, these recordings are expected to be very accu-rate for all herds in the NDHRS. Also, as the reporting of dead farm animals is mandatory according to tax authorities, differences between mortality rates in the NDHRS herds and the survey herds are most likely not due to underreporting from the NDHRS herds.

Risk Factors

Disease and Postmortem Findings. Calves pre-viously diagnosed with arthritis had the highest risk



Figure 2. Survival distribution function for calf mortality in 125 Norwegian dairy herds including calves (n = 5,104) previously registered with (…) or without (—) respiratory disease during their first year of life. The periods used in the analysis (1 to 7 d, 8 to 30 d, 31 to 180 d, and 181 to 365 d of age) are marked with arrows.

of death during the first 6 mo of life, although diar-rhea and respiratory disease were the most frequently reported diseases. Infectious arthritis could be second-ary to an umbilical infection in young calves, and a concurrent septicemia might result in death (Agerholm et al., 1993; Virtala et al., 1996). Few studies have ex-amined risk factors influencing mortality after 180 d of age. Similar to findings of Waltner-Toews et al. (1986), calves that had been treated for respiratory disease had significantly increased risk of death in the current study

(Table 9). Calf diseases in the NCHRS are unfortunate-ly underestimated by approximately 40% (Gulliksen et al., 2009). Therefore, it seems probable that the effect of disease on calf mortality rates is more pronounced than could be demonstrated in this study.

Pneumonia was the most common cause of death among all animals necropsied in the survey, whereas enteritis was the most common diagnosis in the young-est calves. Other studies investigating calf mortality have reported similar findings (Agerholm et al., 1993;



Table 10. Main postmortem diagnosis in 65 calves that died in 37 Norwegian dairy herds participating in a survey on calf health from 2004 to 2008

Diagnosis Calves (n) Proportional rate Mean age (d) Median age (d)

Bronchopneumonia 18 27.7 100.9 101Enteritis 10 15.4 70.3 29.5Chronic indigestion 8 12.3 52 38Omphalophlebitis with pyemia, peritonitis, or multifocal hepatitis 4 6.2 20.5 22Bacteremia/septicemia 4 6.2 37.3 39Ruminal bloat 2 3.1 107.5 107.5Weakborn with bronchopneumonia or bacteremia 2 3.1 18 18Arthritis, purulent 2 3.1 51 51Mesenteric torsion 2 3.1 35 35Abomasal dilatation and peritonitis 1 1.5 32 32Abscess in parotis region 1 1.5 249 249Peritonitis 1 1.5 5 5Pyelonephritis 1 1.5 45 45Small intestine invagination 1 1.5 118 118Inconclusive 8 12.3 38.6 17.5Sum 65 100.0

Figure 3. Survival distribution function for calf mortality in 125 Norwegian dairy herds including calves (n = 5,104) born during 2005 previ-ously registered with (…) or without (—) diarrhea. The periods used in the analysis (1 to 7 d, 8 to 30 d, 31 to 180 d, and 181 to 365 d of age) are marked with arrows.

Svensson et al., 2006; USDA, 2007), and these data are similar to registrations in the NDHRS.

Housing. Calves born in free stalls had a higher risk of stillbirth than calves born in tie stalls. In 19 of 53 (35.8%) free stalls, more than 80% of all calvings oc-curred in the cubicle section or in the alley area. Previ-ous studies of calving management in Norwegian dairy herds have also reported this observation (Kjæstad and Simensen, 2001). If the calf were not removed from the alley area immediately after birth, it would be exposed to high levels of infectious agents from manure and bedding. This is expected to increase the risk of disease and death in the newborn calves. All tie-stall herds included in the survey (n = 71) reported that >80% of all calvings happened while the cow was restrained. Supervision of each cow is easier in tie stalls than in loose housing systems. This could be part of the reason that calving in a tie stall was not found to be a risk fac-tor for stillbirth. According to Norwegian regulations, one maternity pen is required per 25 cows. It is recom-mended that cows be transferred to the maternity unit at least 24 h before expected calving to avoid prolonged calvings due to elevated stress levels and to fulfill the natural, isolation-seeking behavior of calving cows (Bao and Giller, 1991). Larger herd sizes and new housing systems are likely to reduce the possibility of individual supervision of cows in late gestation, and thereby the risk of calvings happening outside maternity pens will increase. Insufficient monitoring around parturition and a high number of unassisted calvings could increase the risk of stillbirth (Lombard et al., 2007; Gundelach et al., 2009).

Suckling calves had an increased risk of death during the first week of life. Although the presence of the dam has been found to increase the amount of IgG absorbed (Quigley et al., 1995), calves left to suckle their dams often fail to ingest adequate volumes of colostrum (Franklin et al., 2003). Svensson et al. (2003) found an increased risk of diarrhea in calves that received colostrum from suckling compared with calves that were given their first meal by the farmer. Wells et al. (1996) found that leaving the calves with the dam for more than 24 h increased the odds of mortality during the following 21 d.

This study indicates that housing calves in a group pen during the first month of life is disadvantageous compared with housing calves in individual pens, as has been reported by Svensson and Liberg (2006). Calves in group pens are likely to experience greater exposure to higher levels of infectious agents earlier in life than calves housed individually, which may result in increased infection and death rates. Svensson et al. (2006) and Svensson and Liberg (2006) found that be-ing housed in group pens was associated with an in-

creased risk of respiratory disease, lower age of onset of diarrhea, and more severe cases of diarrhea compared with calves housed in individual pens. However, group housing enables social interactions between calves and fulfills their needs for motion and play, and is therefore considered preferable from a welfare point of view. Our results indicate that infection status among calves in a herd should be included in the animal welfare debate on optimal housing systems for calves.

Calving Difficulties and Congenital Defects. Calving difficulties and congenital defects were found to be, by far, the most important factors influencing the risk of stillbirth and death during the first week of life, and other studies have reported similar findings (Wells et al., 1996). A calf dying before delivery could also be a reason for calving difficulties. Calves that have undergone a prolonged and difficult birth often experience respiratory problems and weakness, which may result in the period from birth to first colostrum intake being prolonged and colostrum intake being reduced. These factors could result in insufficient in-gestion of IgG, thereby increasing disease susceptibility and mortality risk. Calving difficulty and stillbirth have been part of the total merit index used for selection of Norwegian Red sires since 1978 (Geno, 2008). Accord-ing to Heringstad et al. (2007), the mean frequency of stillbirth has remained unchanged from 1978 to 2004, as has the proportion of calvings reported as “difficult.” The results of the present study indicate that the rea-sons for calving difficulties are complex, but improved management practices around calving and increased calving supervision would probably be beneficial.

Twins and Triplets. According to the current study, twinning is undesirable in dairy cattle production be-cause of increased calf mortality rates during the first month of life. Mee et al. (2008) also found significantly increased risk of perinatal mortality in twins compared with singletons (OR = 13.4 in first-parity cows), and Silva del Río et al. (2007) concluded that cows with twins had a higher incidence of abortion, calving dif-ficulties, retained placenta, and metritis. The influence of twinning on abortion risk could not be included in the current study because for the majority of aborted calves in the NDHRS there is an absence of registration on whether they were singletons, twins, or triplets.

Calving Season. The abortion rate showed both seasonal and geographical variation, being highest during summer and most pronounced in the western part of Norway. The tick Ixodes ricinus is more wide-spread in this region (Stuen et al., 2002) and could cause infections such as anaplasmosis during summer. Anaplasmosis could be a significant cause of abortion in these areas and this possibility should be followed up by further studies. Calving during summer or autumn,



however, was found to reduce the risk of death during the first week and the first month of life. Similar results were reported by Svensson et al. (2006) and Silva del Río et al. (2007), who found that calf mortality rates were lower during warm months compared with cold months. Gulliksen et al. (2008) found that Norwegian dairy cows calving during winter months produced colostrum with a significantly lower IgG content than cows calving during any other season of the year, and colostrum of the highest quality was produced by cows calving during autumn. Thus, there seems to be a rela-tionship between seasonal variation in colostrum qual-ity and calf mortality.

Herd Size. Calf mortality rate increased with in-creasing herd size in all age groups, as has previously been reported in numerous other studies (Lance et al., 1992; Silva del Río et al., 2007). However, this contrasts with results from the NAHMS (USDA, 2002, 2007) in which large operations (>500 cows) had a lower per-centage of unweaned heifer deaths compared with small (<100 cows) and medium-sized (100 to 499 cows) herds, although large herds had a higher percentage of abor-tions. When comparing these studies, it should be noted that Norwegian dairy herds are generally considerably smaller than the herds included in both USDA studies. As herd size increases and there is more mechanization and technological developments used in the cattle in-dustry, the time physically spent in the barn decreases and the daily inspection of each individual animal is re-duced. These factors could contribute toward increased mortality rates.

Parity. Studies from Sweden (Berglund et al., 2003), Ireland (Silva del Río et al., 2007), and North America (Meyer et al., 2000) indicate that bovine perinatal mortality rates are increasing, particularly in Holstein heifers. Feto-pelvic disproportion has an effect on still-births, and the increased risk of stillbirth in primipa-rous cows could be due in part to a higher frequency of calving difficulties. Nevertheless, the risk of stillbirth was still significantly higher in primiparous cows when only those calvings reported as normal were included in the analyses.

Other Risk Factors. The lower risk of stillbirth in the Norwegian Red breed compared with other breeds or crossbreeds is likely to be a result of numerous years of genetic selection for sires with low stillbirth rates (Heringstad et al., 2007). In addition, the use of beef cattle sires in crossbreeding might lead to feto-pelvic disproportion, and thereby a higher risk of calving dif-ficulties.

No difference in stillbirth risk between male and fe-male calves was shown in our study, which is in contrast to the results of the studies of Chassagne et al. (1999) and Meyer et al. (2001), who found that bull calves

were more likely to be stillborn than heifer calves. Sex is not recorded for the majority of aborted and stillborn calves in the NDHRS, and therefore interpretation of the results concerning sex of calf as a potential risk factor for abortion and stillbirth is difficult when using data from this database.

Significant cluster effects within herd were found in all age groups. The OR varied between 2.13 for still-birth and 3.59 for death between 180 and 365 d of life. This implies that, in addition to management factors, the occurrence of infectious agents within each herd is important in the variation in risk of calf mortality.

COnCLuSIOnS

Calves diagnosed with diarrhea, respiratory disease, or arthritis had a significantly increased risk of death. This study indicates that individual housing and man-ual feeding of colostrum are preferable to group housing and suckling during the first 4 wk of life. To reduce calf mortality in Norwegian dairy herds, attention should be focused on those risk factors that are under man-agement control. Efforts should be made to increase calving supervision, improve management of newborn calves, and prevent respiratory diseases and diarrhea.

aCKnOWLeDGmentS

The authors thank all the participating farmers, vet-erinarians, and laboratory personnel for their involve-ment in the current research. The study was funded by TINE Norwegian Dairies BA (Ås, Norway), Animalia (Løren, Norway), and the Research Council of Norway (Oslo). Access to production and health data was given by the Norwegian Dairy Herd Recording System and the Norwegian Cattle Health Services in agreement number 8/2002.

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Calf mortality in Norwegian dairy herds · and weaned heifers, respectively (USDA, 2007). Sim-ensen (1982a) reported a mortality rate of 4.0%, includ-ing stillbirth, during the first

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