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Variance components of clinical mastitis in dairy cattle —
effects of trait definition and culling
*
Bjørg Heringstad , Gunnar Klemetsdal, John Ruane
˚Department of Animal Science, Agricultural University of Norway, P.O. Box 5025, N-1432 As, Norway Received 17 May 1999; received in revised form 28 March 2000; accepted 27 April 2000
Abstract
First lactation clinical mastitis records for Norwegian cattle from 1978 onwards were analysed. Variance components for clinical mastitis were estimated with a linear sire model using records of more than 500,000 daughters of 2043 sires. Heritability increased slightly as the period for sampling health data increased, and the longest period analysed (from 15
2
days before calving to 210 days after calving) gave the highest heritability estimates (h 50.04). However, a sampling
2
period from 15 days before calving to 30 days after calving captured most of the genetic variation (h 50.03), and showed a high genetic correlation (.0.94) with clinical mastitis sampled over a longer period of first lactation. This implies that recording of clinical mastitis over a short time period around first calving can provide a measure of clinical mastitis with a substantial value in genetic evaluation. Using culling reason as an additional source of information about mastitis increased heritability only slightly compared with using clinical mastitis records only. Excluding cows culled before the end of the sampling period from the data if they have not had mastitis resulted in a higher heritability of mastitis than both including a fixed effect to account for culling in the model and a bivariate analysis of clinical mastitis and culling. Hence, culling affects variance component estimates of clinical mastitis. 2001 Elsevier Science B.V. All rights reserved.
Keywords: Dairy cattle; Clinical mastitis; Genetic parameters
1. Introduction Norway together with Denmark, Finland and Sweden
are the only countries with national recording sys-Breeding for increased mastitis resistance is one tems for health data and the only countries which strategy to reduce mastitis, which is the most fre- include clinical mastitis resistance directly in their quent and costly disease affecting dairy cattle. A dairy cattle breeding programs (Heringstad et al., reduced mastitis frequency will reduce costs of 2000).
production, reduce the use of antibiotics and is In genetic evaluation, all four Nordic countries use important for ethical and animal welfare reasons. field records of veterinary-treated cases of clinical mastitis. Generally, mastitis is considered as an all-or-none trait, cows being categorised as diseased if
*Corresponding author. Tel.:147-6494-8000; fax:1
47-6494-they had mastitis in a defined period of lactation and
7960.
E-mail address: [email protected] (B. Heringstad). as healthy if there was no report of mastitis in this
period. The relevant period varies between countries, Recording System, from 1978 onwards (described by covering the period of 10 days before to 180 days Ruane et al., 1997). As in Heringstad et al. (1999), after calving in Denmark, 7 days before to 150 days data extraction was carried out by combining in-after calving in Finland, 15 days before to 120 days formation in a pedigree file with information on after calving in Norway and 10 days before to 150 clinical mastitis and culling. In building up the data days after calving in Sweden (Heringstad et al., sets, a record was included if first calving was 2000). To avoid bias due to culling of cows, between 1 September 1978 and 31 December 1995, information from only a short period of lactation is age at first calving was between 450 and 1200 days used. In Danish clinical mastitis data, the highest and the lactation started with a normal calving (i.e. heritability was found when using data from 10 days lactations starting with an abortion or with a calving before to 50 days after first calving (Lund et al., in another herd were omitted). To ensure participa-1999) tion in the health recording system, only data from For genetic evaluation in Finland and Sweden, herds with at least one disease record during the year culling due to udder health problems (reported by the the cow calved were accepted.
farmer) is used as additional information about First lactation clinical mastitis information, from mastitis (Heringstad et al., 2000). Koenen et al. 15 days before calving to 210 days after calving (or (1994) found significantly higher heritability esti- to date of culling if less than 210 days after calving), mates for mastitis in Swedish data when such was stored by use of two variables; dates of the last information was utilised. In Norway, culling reasons mastitis observation before calving and the first have been reported by farmers since 1978, but were mastitis observation after calving. Additionally, cul-initially not sufficiently defined to be of value in ling date and culling reason were kept for cows genetic evaluation. Since 1989, however, ‘high culled during the first lactation, from 1989 onwards. somatic cell count (SCC) / mastitis’ has been ‘High SCC / mastitis’ was not a category of culling specified as a category of culling reasons, and this reason for cows culled before 1989 (37% of cows). information can be used in genetic analyses of Finally, information was limited to daughters of mastitis. Culling reason potentially makes it possible young bulls progeny tested in the years 1978 to to identify cows with mastitis that are culled instead 1995. Only first crop daughters were used, and of being treated. records of A.I. sires with less than 20 daughters were The first aim of this study was to study the effect deleted. The resulting data file included a total of of length of the sampling period of health data on the 549,995 first lactation daughters bred by 2043 sires, heritability of clinical mastitis and to estimate the from 253,371 different herd by year classes. genetic correlations between clinical mastitis from
different sampling periods. The second aim was to 2.2. Trait definition examine whether inclusion of culling reason as an
additional source of information about mastitis af- Eight different data sets were created to study the fected the heritability estimate. The third aim was to effect of the length of the sampling period of health perform an introductory study of the effect of culling data on the heritability of clinical mastitis. Clinical of cows before the end of the sampling period on mastitis (CM) was defined as a binary trait, on the variance component estimates. basis of whether or not the cow had had clinical mastitis in the period from 15 days before first calving to date of calving (0) or to 30, 60, 90, 120,
2. Material and methods 150, 180 or 210 days after calving.
the relevant period were classified as diseased, if the all cows were classified as culled or not before 120 culling reason reported by the farmer was ‘high days after calving. The second strategy to account SCC / mastitis’, even if the cows did not have a for culling is to define culling before 120 days after record of mastitis treatment. calving as a binary trait, and to use data set In all, 16 data sets, data on cows culled before the CM120FIX in a bivariate analysis of clinical mastitis end of the relevant period, were included if they and culling (05not culled; 15culled). The structure were classified as diseased. If not, they were ex- of the CM120FIX data set is given in Table 2, which cluded, since cows culled before the end of the also gives information on CM120 (defined in Section period were not considered to have had a sufficient 2.2) for comparison purposes. In CM120, the 35,967 chance to express the trait. The number of records cows culled before 120 days after calving and and mastitis frequencies in the 16 data sets are given classified as healthy are excluded, while they are in Table 1. CMCR data sets have at most 2739 included in CM120FIX.
additional records compared to their CM equivalents.
Estimation of genetic correlations between clinical 2.4. Sire pedigree file mastitis from different sampling periods was limited
to CM0, CM30, CM120, and CM210. A sire pedigree file was constructed by tracing the pedigree of the 2043 bulls appearing as sires in the 2.3. Culling of cows before the end of the data files as far back as possible. The pedigree file
sampling period contained a total of 2159 bulls, the first born in 1940.
In total, 50 bulls had unknown sires, and were Instead of simply omitting data on cows that were assumed to represent the base population.
culled before the end of the sampling period and that were classified as healthy, two strategies for
includ-2.5. Model ing the data were considered. The first is to include a
fixed effect of culling (two classes) in the model, as
Variance components for mastitis were estimated currently done in genetic evaluation of mastitis in
using the following linear sire model: Norway. To examine the effect of this approach on
variance components, a data set CM120FIX was Y 5A 1M 1HY 1 S 1E
ijklm i j k l ijklm
created. As before, clinical mastitis was considered
as a binary trait, on the basis of information in the where Yijklm is an observation of mastitis (05no period from 15 days before to 120 days after first mastitis; 15mastitis), A is the fixed effect of the ithi calving. Culled cows were kept in the data set, and age at calving in 15 classes, where ,20 months is
Table 1
Number of records and mastitis frequencies in the 16 data sets used to study the effect of the sampling period on variance component a estimates for traits defined on the basis of clinical mastitis only (CM) or, in addition, using information on culling reason (CMCR)
End of sampling Clinical mastitis (CM) Clinical mastitis and culling reason (CMCR) period, days after
Data No. of Mastitis Data No. of Mastitis
b first calving
set records frequency (%) set records frequency (%)
0 CM0 549,995 3.5 CMCR0 549,995 3.5
30 CM30 537,902 11.2 CMCR30 538,714 11.4
60 CM60 529,430 12.9 CMCR60 530,596 13.1
90 CM90 521,918 14.4 CMCR90 523,341 14.7
120 CM120 514,028 15.9 CMCR120 515,754 16.2
150 CM150 505,087 17.3 CMCR150 507,136 17.7
180 CM180 494,967 18.7 CMCR180 497,371 19.1
210 CM210 484,351 20.0 CMCR210 487,090 20.5
a
For both CM and CMCR, cows culled before the end of the sampling period were excluded if classified as healthy. b
Table 2
Summary statistics of the data set CM120FIX used for the bivariate analysis of mastitis and culling and to examine the effect of accounting for culling as a fixed effect on variance component estimates of clinical mastitis. The sampling period was from 15 days before to 120 days after first calving, and the reference data set CM120 was defined as in Table 1
a
CM120FIX CM120
Number of records 549,995 514,028
Number of sires 2043 2043
Number of herd3year classes 253,371 246,960
Mean number of daughters per sire 269 252
Mean number of records per herd3year 2.2 2.1
Mastitis frequency (%) 14.9 15.9
Year of calving 1978–1995 1978–1995
a
A total of 8.7% of the cows were culled before 120 days after first calving.
2
the first class and .32 months the last class, and the reasonably high (h 50.033 and 0.034). It is also other classes are in single months, M is the fixedj interesting to note the heritability of 0.016 when the effect of the jth month of calving in 12 classes, HYk sampling period ended at the day of first calving. is the fixed effect of the kth herd by year class, S is1 Heritability estimates for CM120, CM150 and the random effect of the cth sire, and Eijklm is a CM180, which correspond to the sampling periods random error term. used in Norway, Finland and Sweden, and Denmark, An additional fixed effect was included in the were 0.037, 0.039 and 0.040, respectively. Heritabili-univariate analysis of data set CM120FIX: C is the ty estimates transformed to the underlying scale were fixed effect of culling or not before 120 days after fairly constant, between 0.084 and 0.092. Estimates calving, in two classes (05not culled; 15culled). In of heritability from CMCR were slightly higher than the bivariate analysis of clinical mastitis and culling, from CM on both the observable and underlying and in the bivariate analyses of clinical mastitis from scale.
different sampling periods, the same model as in the Table 3 shows the estimated variance components univariate analyses was assumed for both traits. for clinical mastitis (CM) and the mastitis variable An additive relationship matrix containing the where the trait is defined on the basis of clinical relationship between sires was included in the analy- mastitis and culling reason (CMCR), for different ses. Variance components for random effects were length of the sampling period. Both the sire and the estimated with REML, using the program VCE4 residual variance components increase with increas-(Neumaier and Groeneveld, 1998). Heritability esti- ing sampling period. Sire variance increases rela-mates were transformed from the observable 0 / 1 tively more than the residual variance, which results scale to the assumed underlying scale using the in higher heritabilities. The genetic variance was classical formula of Dempster and Lerner (1950). roughly twice as high for sampling periods up to 210 days (CM210 and CMCR210) as for sampling periods ending 30 days after calving (CM30 and
3. Results CMCR30).
The estimated genetic correlations between clini-Fig. 1 shows that heritability estimates on the cal mastitis measured in different time periods of the observable scale for both mastitis variables (CM and first lactation are shown in Table 4. Genetic correla-CMCR) increase with the length of the sampling tions between CM30, CM120, and CM210 were all period, and that the period from 15 days prior to high (.0.94). The genetic correlations between calving to 210 days after calving resulted in the mastitis prior to calving (CM0) and the other CM
2
highest heritability estimates (h 50.042 and 0.043, variables were between 0.84 and 0.94.
sam-Fig. 1. Heritability estimates of clinical mastitis (CM) and a mastitis variable where the trait is defined on the basis of clinical mastitis and culling reason (CMCR) for sampling periods from 15 days prior to first calving to date of calving (0) or to 30, 60, 90, 120, 150, 180 or 210 days after calving. Heritability estimates transformed to the assumed underlying scale (CM-t and CMCR-t) using the formula of Dempster and Lerner (1950) are also included.
Table 3
2
Variance components and heritability (h ) of clinical mastitis (CM) and a mastitis variable where the trait is defined on the basis of clinical mastitis and culling reason (CMCR) for sampling periods from 15 days prior to first calving to date of calving (0) or to 30, 60, 90, 120, 150, 180 or 210 days after calving
Clinical mastitis (CM) Clinical mastitis and culling reason (CMCR)
2 2
Data Sire Residual h Data Sire Residual h
set variance variance set variance variance
a a
CM0 0.00013 0.03339 0.016 CMCR0 0.00013 0.03339 0.016
b b
CM30 0.00078 0.09325 0.033 CMCR30 0.00080 0.09432 0.034
b b
CM60 0.00092 0.10449 0.035 CMCR60 0.00095 0.10592 0.036
b b
CM90 0.00103 0.11429 0.036 CMCR90 0.00107 0.11594 0.037
b b
CM120 0.00115 0.12314 0.037 CMCR120 0.00120 0.12504 0.038
b c
CM150 0.00128 0.13123 0.039 CMCR150 0.00134 0.13338 0.040
c c
CM180 0.00141 0.13877 0.040 CMCR180 0.00147 0.14114 0.041
c c
CM210 0.00154 0.14572 0.042 CMCR210 0.00161 0.14831 0.042
a
Standard error of the ratios (variance component / total variance): 0.0003. b
Standard error of the ratios (variance component / total variance): 0.0004. c
Table 4 4. Discussion Genetic correlations between clinical mastitis variables based on
sampling periods from 15 days prior to calving to the date of
The heritability estimates reported here are in
calving (0) or 30, 120 and 210 days after calving (CM0, CM30,
agreement with previous results. Heritability
esti-CM120 and CM210, respectively) above the diagonal, and the
corresponding standard errors below the diagonal mates of clinical mastitis based on Nordic field data analysed with linear methods on the observable scale
CM0 CM30 CM120 CM210
range from 0.001 to 0.06, with most values in the
CM0 0.94 0.90 0.84
interval from 0.02 to 0.03 (reviewed by Heringstad et
CM30 0.014 0.98 0.94
al., 2000). A linear sire model is currently used for
CM120 0.017 0.003 0.99
CM210 0.020 0.007 0.002 genetic evaluation of mastitis in Norway and was therefore chosen for analyses, although a threshold model would have been more appropriate for
cate-Table 5
gorical data.
Variance components and heritability of clinical mastitis estimated
Heringstad et al. (1999) showed that variance
with two data sets: CM120FIX, analysed using a model with a
components based on first crop daughters only or on
fixed effect to account for culling prior to 120 days after first
calving; and CM120, where cows culled before the end of the all daughters of a sire, given that his first crop
sampling period were excluded if classified as healthy daughters were present in the data, resulted in very
CM120FIX CM120 similar results. Hence, only first crop daughters were
a used in this study to minimise computational needs.
Sire variance 0.00096 0.00115
a A preliminary study of the effect of the sampling Residual variance 0.11573 0.12314
Total variance 0.11669 0.12429 period, using a subset of the current data, showed
Heritability 0.033 0.037 that using information on clinical mastitis before first
a
Standard error of the ratios (variance component / total vari- calving resulted in higher heritability estimates than
ance): 0.0004. if the period started at calving (Heringstad et al.,
1997). However, no major differences were found
Table 6 between starting 10, 20 or 30 days prior to calving.
(Co)variance components for clinical mastitis and culling from a Therefore, only one starting point, 15 days before bivariate analysis of data set CM120FIX calving, was considered here, as it is also the one
Mastitis Culling Mastitis currently used for breeding value estimation in
and culling Norway.
a b
Sire (co)variance 0.00100 0.00028 0.00018 Fig. 1 shows that the heritability estimates
in-a b
Residual (co)variance 0.11664 0.07876 0.00847 crease with longer sampling periods. This was Total (co)variance 0.11764 0.07904 0.00865 expected since mastitis frequency increased from 11 Heritability 0.034 0.014
c to 20% as the sampling end point increased from 30
Genetic correlation 0.334
to 210 days after calving (Table 1), and heritability a
Standard error of the ratios (variance component / total
vari-estimates are frequency dependent when applying
ance): 0.0004.
b linear models to categorical data (Gianola, 1982). To Standard error of the ratios (variance component / total
vari-remove this dependency, heritability estimates were
ance): 0.0003. c
Standard error: 0.037. transformed to the assumed underlying scale (De-mpster and Lerner, 1950). The transformed heritability estimates show flat curves (Fig. 1), pling period from 15 days before to 120 days after indicating that increased heritability estimates for calving, heritability was 0.037 with CM120, while longer sampling periods are an effect of increased CM120FIX, with culling as a fixed effect, yielded a mastitis frequency.
compared heritability estimates based on clinical The joint effect of the increased heritability and mastitis from 10 days before calving to 50, 180 and the changed genetic correlation over time can be 305 days after calving, respectively, and found estimated as a correlated genetic response to selec-higher heritabilities for longer sampling periods on tion by use of simple selection index theory. The the observed scale, although, converted to the under- effect can be illustrated by calculating the expected lying scale, heritability was highest for the shortest genetic superiority in, for example, the sire to son sampling period. These results indicate that relatively path, assuming CM210 as the breeding goal trait. little is gained with respect to size of heritability Under these assumptions the selection responses for from sampling clinical mastitis data from a longer CM0, CM30 and CM120 were 67, 90 and 97%, time period than the first 1–2 months after first respectively, of the response obtained under direct
calving. selection using CM210.
It is likely that a sampling period covering 15 days Including culling reason as an additional source of before first calving to 30 days after calving captures information about mastitis increased the heritability a large part of the genetic variance, since more than estimates only slightly. This was because the inclu-50% of the first cases of clinical mastitis, in a data sion of data on culling reason provided very little set of 1.7 million cows, occurred within the first 30 extra information on the occurrence of clinical days after calving (Heringstad et al., 1999). For the mastitis. Taking the whole period up to 210 days data set analysed in this study, the frequency of after calving (Table 1), only 2739 cows (0.6%) were clinical mastitis up to 30 days after calving (CM30) identified as culled for ‘high SCC / mastitis’ and not was 11.2%, which is not greatly inferior to the recorded for clinical mastitis treatment. This is partly 15.9% incidence that would be analysed in the due to the fact that 37% of the cows were culled current sampling period used in Norway (Table 1). A before 1989 and ‘high SCC / mastitis’ was only further increase of the sampling period past 30 days included as culling reason from that year onwards. It would include more cases of mastitis, but might also may also suggest that the health recording system is introduce a bias due to culling of cows. Lund et al. very efficient or, alternatively, that the culling reason (1999) found heritability on the underlying scale to is being inaccurately recorded by the farmers. It may be highest in early lactation and suggested that also be a problem that, in the Norwegian recording clinical mastitis in the beginning of lactation, when of culling reason, high SCC and mastitis are put the cows’ physiological demands are high, is more together as one category, while SCC and clinical related to the cows genetic resistance to mastitis than mastitis are two different traits with a genetic
¨ ¨ ¨
later in lactation. correlation far from unity (e.g., Poso and Mantysaari, These results have important practical conse- 1996; Lund et al., 1999).
quences. So far, only the four Nordic countries have With Swedish data, Koenen et al. (1994) found a national health recording systems. Although there is much larger effect when including culling reason. considerable interest, it is often considered that Heritability on the observable scale increased from systems for recording clinical mastitis treatments 0.018 to 0.083. The importance of utilising culling would be difficult to establish in other countries (e.g., reason as additional information in breeding against Colleau and le Bihan-Duval, 1995). However, for mastitis will obviously vary between countries and those countries wishing to include clinical mastitis in will depend on recording systems of both health data dairy cattle breeding programs, recording mastitis and reason for culling. Both in this study and in over a very short period of the first lactation could be Koenen et al. (1994) the heritabilities transformed to an alternative that would not be too expensive and the underlying scale were enhanced by utilising that would provide a measure of clinical mastitis culling reason information. This indicates that the with a reasonable heritability value. This argument is increased heritability was not only an effect of further strengthened by the high genetic correlation increased mastitis frequency in the CMCR data sets (0.98) between clinical mastitis observed over 30 but rather that CMCR defines a trait with a slightly days (CM30) and over 120 days (CM120) of the first higher heritability than CM.
culling showed that culling, defined as a categorical but both strategies gave lower heritability estimates trait, had an estimated genetic correlation of 0.33 than simply excluding cows culled before the end of with clinical mastitis (Table 6). Hence, including the sampling period if they did not have mastitis. culling as a fixed effect (the univariate analysis) Hence, culling affects variance component estimates reduces the genetic variance and the heritability of of clinical mastitis.
clinical mastitis compared with a bivariate analysis of the two traits (Tables 5 and 6). The increased heritability of mastitis indicates that a bivariate
Acknowledgements analysis accounts better for culling than including a
fixed effect of culling in the model. However, simply
The Norwegian Dairy Cattle Recording System excluding cows culled before the end of the sampling
(Husdyrkontrollen / NML) is acknowledged for pro-period that were not classified as diseased (CM120)
viding data and GENO Breeding and A.I. Associa-resulted in a higher heritability than the two other
tion for providing pedigree information on bulls. approaches. The advantage of this strategy is that
mastitis can be analysed by a univariate model. The disadvantage is that there is some selection in the
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