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Incidence and heritability of ovine pneumonia, and the relationship with production traits in New Zealand sheep
Small Ruminant Research 145 (2016) 136–141
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Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Incidence and heritability of ovine pneumonia, and the relationship with production traits in New Zealand sheep Kathryn M. McRae, Hayley J. Baird, Ken G. Dodds, Matthew J. Bixley, Shannon M. Clarke ∗ AgResearch Invermay, Private Bag 50034, Mosgiel 9053, New Zealand
a r t i c l e
i n f o
Article history: Received 28 April 2016 Received in revised form 3 August 2016 Accepted 4 November 2016 Available online 8 November 2016 Keywords: Sheep Pneumonia Heritability Disease
a b s t r a c t The cost of ovine pneumonia and pleurisy to the New Zealand economy is high, with the majority of loss through slower growth and reduced carcass value at slaughter. Farm management practices and vaccine development have traditionally been the main focus for prevention of pneumonia. The objective of this study was to estimate the heritability of pneumonia in New Zealand lambs, and investigate the genetic relationship with key production traits. The lungs of 11,437 lambs from pedigree-recorded flocks were scored for the presence and severity of pneumonic lesions at slaughter. On average 28% of lambs had pneumonic lesions at slaughter, with 7% showing severe lesions. The incidence of pleurisy in these animals was 6%. Heritability estimates for pneumonic lesions and pleurisy were 0.07 ± 0.02 and 0.02 ± 0.01, respectively. There was a significant positive genetic correlation between pneumonic lesions and faecal egg count (0.30 ± 0.13). Animals with pneumonic lesions had grown faster from birth to weaning, and slower from weaning to slaughter than animals without lesions. This study has shown that there is a heritable component to pneumonia in sheep. Including more data from pedigree-recorded flocks with severe pneumonia and a high incidence of pleurisy will enable more accurate estimates of genetic parameters, and subsequent correlations with production and disease traits. This would be aided by routine recording of pneumonia in lungs at slaughter by processing plants. © 2016 Published by Elsevier B.V.
1. Introduction Respiratory diseases, including pneumonia, are common in most livestock around the world. The economic cost of pneumonia to the New Zealand sheep industry is high and consists of three main factors; direct losses of stock on farm, reduced weight gains and wool production from sub-clinical animals, and condemnation and downgrading of carcasses at slaughter (West et al., 2009). A study by Goodwin-Ray et al. (2008c) estimated the annual cost of pneumonia to the New Zealand sheep industry to be NZD$1.36 to $3.31 per lamb, with the prevalence of pneumonia during February through April having the greatest impact on cost. However, this is a conservative estimate of the cost to the industry given the study did not include the costs associated with pneumonia related mortalities on farm. Pneumonia has been reported to have a significant effect on lamb growth rate (Kirton et al., 1976; Alley, 1987; Goodwin et al., 2004). The extent of the loss depends on the study; the first study of its kind in New Zealand sheep
∗ Corresponding author. E-mail address: [email protected] (S.M. Clarke). http://dx.doi.org/10.1016/j.smallrumres.2016.11.003 0921-4488/© 2016 Published by Elsevier B.V.
by Kirton et al. (1976) showed that when adjusted for weaning weight moderate to severe pneumonia reduced carcass weights by 450 g. Alley (1987) found that carcass weights of lambs with experimentally-induced chronic non-progressive pneumonia were on average 1.5 kg lighter than controls over a 2 month period. Goodwin et al. (2004) addressed the relationship between severity of pneumonia and average daily gain (ADG) in the month prior to slaughter, finding that when more than 20% of the lung surface area was affected by pneumonia, ADG decreased from 136 to 65 g/day. In sheep respiratory disease is etiologically complex, resulting from an interaction of the infectious agents (bacterial, mycobacterial, and viral) with the host’s defence mechanisms, which are often compromised by environmental factors (Alley, 2002). In New Zealand the term chronic non-progressive pneumonia (CNP) is typically used to describe subclinical pneumonia, which is widespread among lambs (Goodwin et al., 2004). Acute pneumonia occurs more sporadically, and occurs in sheep of all ages. The disease has a rapid onset and the first sign is often the death of the affected animal, although recovery with chronic lesions may also occur (Alley, 2002). Animals that have subclinical pneumonia and those that have survived clinical pneumonia may develop pleurisy, where the lungs adhere to the chest wall.
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Clinical diagnosis of pneumonia is difficult, with accurate diagnosis requiring post-mortem examination of the lungs; hence the animal needs to be euthanised. Traditionally, the main focus for prevention of pneumonia has been farm management practices and vaccine development. A case-control study by Goodwin-Ray et al. (2008a) identified shearing lambs at weaning, breeding replacement ewes on farm and contact with other flocks through the purchase of lambs post-weaning as practises likely to increase pneumonia prevalence. Vitamin B12 treatments at time of docking and weaning, as well as set stocking lambs post-weaning, were seen as protective practises. Lambs slaughtered later in the season versus at or around the time of weaning are at much higher risk, but this is more likely to be a consequence of slower growth because of pneumonia than a cause of pneumonia. A vaccine based on the serotype S1 strain of Mannheimia haemolytica, the primary cause of lung damage, has been shown to provide cross-protection against S2 strains in an experimental challenge (Zheng et al., 2015). The evaluation of a commercial vaccine containing antigens of M. haemolytica and Pasteurella trehalosi (Ovipast Plus, Intervet) under field conditions showed no difference in prevalence of pneumonic lesions or ADG between the placebo-treated and vaccinated lambs (Goodwin-Ray et al., 2008b). Improvement of animal health through genetic selection can provide a complementary approach to disease control (Stear et al., 2001; Bishop and Morris, 2007; Berry et al., 2011). Baird et al. (2012) developed a pneumonic lesion scoring system in the processing plant (chain speed), and estimated the heritability of the consolidated pneumonic lesion score in pedigree-recorded lambs to be 0.12 ± 0.06. This is comparable to estimates of heritability of bovine respiratory disease (BRD) resistance in cattle, which range from 0.04 to 0.26 (Muggli-Cockett et al., 1992; Snowder et al., 2005; Schneider et al., 2010). The objective of this study was to expand on previous work to estimate the heritability of pneumonic lesions in New Zealand lambs, and, in addition, investigate the genetic relationship with key production traits
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lungs were fresh. For lambs born 2008–2010 this was determined by removing the lungs from the processing chain and visually assessing each of the five lobes. Each lobe was scored on a 0–5 scale, indicating the percentage of surface area affected, where 0 = no lesions present; 1 = small lesions; 2 = approximately 25% of the lobe affected; 3 = approximately 50% of the lobe affected; 4 = approximately 75% of the lobe affected and 5 = 100% of the lobe affected. Pneumonic lesions were defined as compacted, dark purple-red areas of the lung that were firm to touch (Fig. 1B and C). The sum of the individual lobe scores was calculated and recorded as a ‘total lesion score’ (TLS). The TLS system is not appropriate for recording pneumonic lesions at chain-speed on the processing chain at the plant, where up to 10 animals per minute may be slaughtered. A refined scoring system was devised by Baird et al. (2012) and was implemented for recording pneumonic lesions at chain-speed from the progeny born in 2011 onwards. This refined TLS system, termed ‘consolidated pneumonia score’ (CPS), has a range from 0 to 2, where 0 = no lesions present; 1 = any individual lobe with up to 50% of the lobe affected and 2 = any individual lobe with greater than 50% of the lobe affected (Fig. 1). Animals that had been scored under the TLS system were retrospectively given CPS values, and CPS was used for all subsequent analysis. 2.3. Production Traits Carcass weight (CWT), and primary and secondary carcass fault data, including pleurisy (PLEUR) were obtained from the meat processing plant. The carcass measurements of depth of tissue 110 mm off the mid line in the region of the 12th rib (CGRM) and carcass butt circumference (CBUTT) were measured the day post-slaughter, before the further processing of the carcass. All other data, including Julian date of birth (JDOB), birth rearing rank (BRR; born as a single, twin or triplet, and raised as a single, twin or triplet), age of dam AOD; (1 year old, 2 years old, or older), birth weight (BWT), weaning weight (WWT), weaning weight mob, pre-slaughter weight (PRESLTWT), pedigree, date of slaughter and breed were obtained from Sheep Improvement Limited (SIL) records.
2. Materials and methods 2.4. Statistical analysis The work reported here was undertaken using records sourced from New Zealand sheep breeders and stored in the Sheep Improvement Limited database (SIL, www.sil.co.nz). The animals were managed in accordance with the provisions of the New Zealand Animal Welfare Act 1999, and the New Zealand Codes of Welfare developed under sections 68–79 of the Act. 2.1. Animals The lungs from a total of 11,437 ram and ewe lambs from one North Island (Flock H) and eight (Flocks A–G and I) Southland and Otago pedigree-recorded flocks were scored for the presence and severity of pneumonic lesions. Data collection was carried out from January to May. Animals from flocks I and E were selected for slaughter by weight and body condition score at 3 different time points. Pneumonic lesions were only recorded in lambs slaughtered at the second and third time points, as preliminary studies had shown little to no lesions in the lungs of lambs slaughtered at weaning. All other flocks were fixed-date slaughters, and primarily took place between February and March. Animals were predominantly composites of the main dual-purpose sheep breeds used in New Zealand, including Romney, Coopworth, Perendale, and Texel. 2.2. Pneumonia scoring system The extent of the pneumonic lesions within the lungs was determined post-slaughter at the processing plant, ensuring the
Data cleaning consisted of removal of records with 1) missing values for sire information or weaning weight, and 2) contemporary groups containing less than 5 observations. Weight and slaughter traits were adjusted using SIL standard practice (S-A. Newman, personal communication) to account for relationships between contemporary group mean and variance, using the equation: aTr = (Tr/Trm)*oTrm where Trm is the mean for the contemporary group, and oTrm is the overall mean for the trait (Brown et al., 2005). Contemporary group (CG) was specific to each trait, and was defined as flock, birth year, sex, weaning mob and trait/slaughter mob combination. The traits adjusted using this approach were BWT, WWT, PRESLTWT, CWT, CBUTT and CGRM. Summer faecal egg count values are a repeatable trait, and were estimated from two samples, taken several days apart. These were distinguished as Nematodirus (NEM1) or ‘other trichostrongyles’ (FEC1; primarily Teladorsagia spp, Trichostrongylus spp and Cooperia curticei). Both FEC1 and NEM1 values were log transformed before analysis (ln(X + 25)). To account for lack of challenge in some contemporary groups (CGkill; sex, birth year, flock, weaning mob and kill date), data was set to missing if the mean CPS in that contemporary group was below 0.1. This is assuming that animals in the contemporary groups where CPS was low were not sufficiently exposed to stressors and pathogens to express a phenotype. To adjust for heteroscedasticity, CPS (initially scored as 0, 1 or 2) was scaled using the formula CPSa = CPS/SQRT(CPSm*(2-CPSm)), where m is the
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Fig. 1. Consolidated pneumonia score (CPS) scoring system. Pneumonic lesions were defined as compacted areas of the lung that are dark purple-red in appearance, and firm to touch (examples shown by arrows). Lungs were scored as 0 = no lesions present (A); 1 = any individual lobe with up to 50% of the lobe affected (B) or 2 = any individual lobe with greater than 50% of the lobe affected (C).
incidence rate per contemporary group (CGkill). Pleurisy (initially coded as 0 or 1) values were also transformed using the formula PLEURa = PLEUR/SQRT(PLEURm*(1-PLEURm)). Data analysis models were determined for each trait separately using forward and backward selection in R. Model selection and comparison was conducted using the Bayesian Information Criterion (BIC) and R2 . Fixed effects fitted included trait contemporary group, birth-rearing rank, and age of dam fitted as linear (AOD) and quadratic (AOD2 ) effects. Birthday deviation (BDEV) from the mean of the contemporary group (CGweaning: sex, flock, year and weaning mob) was calculated using JDOB and fitted as a covariate. The final dataset used in the analysis contained records for 11,409 lambs, and the final models are presented in Table 1. The relationship between growth rates and untransformed CPS was examined using the GLM procedure in SAS (SAS Institute Inc., Cary NC, USA), additionally fitting BDEV, BRR, AOD and contemporary group in the model. Variance and covariance components were estimated using restricted maximum likelihood (REML) procedures fitting an animal model in ASReml (Gilmour et al., 2009), with maternal and permanent environmental effects fitted when appropriate (Table 1). Heritabilities were obtained from univariate analyses of the respective traits, and genotypic and phenotypic correlations between traits were obtained from bivariate analyses.
3.2. The effect of pneumonia on growth and carcass weight Table 2 shows the least squares means (± standard error) of growth rates and CWT classified by CPS. Animals with pneumonic lesions (CPS > 0) at slaughter had grown faster from birth to weaning (P < 0.001), and slower from weaning to pre-slaughter (P < 0.01) than animals without lesions. There was no difference in growth rate between animals scored as 1 or 2 from birth to weaning, however animals with a CPS of 2 grew more slowly than animals with a CPS of 1 from weaning to slaughter (P < 0.001). Animals with more than 50% of a lobe affected by pneumonic lesions (CPS = 2) grew more slowly from birth to slaughter and had a lower carcass weight than both those with less than 50% affected (CPS = 1) or no pneumonic lesions (CPS = 0; P < 0.01). 3.3. Genetic parameters Heritabilities and correlations are presented in Table 3. The heritability estimates for CPSa and PLEURa were 0.07 ± 0.02 and 0.02 ± 0.01, respectively. The genetic correlation between CPSa and FEC1 was significant and positive (0.30 ± 0.13). Neither CPSa nor PLEURa were significantly genetically correlated with any other measured trait, including liveweights or carcass measurements.
3. Results
4. Discussion
3.1. Incidence of pneumonia and pleurisy
Investigation of the genetic relationships underlying complex traits such as pneumonia requires the collection of prevalence data from a large number of pedigree recorded flocks. The development of a visual scoring system of lungs for pneumonic lesions that can be implemented at the processing plant (Baird et al., 2012) was utilised to examine the incidence of pneumonic lesions at slaughter, and the effects on production traits. The average incidence over all of the years measured was 28%. This is higher than the 21.8%
The incidence of pneumonic lesions and pleurisy was recorded for 11,471 lambs born between 2008 and 2014 (Fig. 2 and Supplementary Table 1). The overall incidence of pneumonic lesions (CPS of 1 or 2) was 28% (range 9%–52% over cohorts), with an average of 7% (range 0%–18%) of animals having a score of 2. The incidence of pleurisy in these animals was 6% (range 0%–16%).
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Table 1 Descriptive unadjusted statistics and final mixed models used for individual trait analysis. Descriptive analysis a Trait
b
BWT (kg) WWT (kg) PRESLTWT (kg) avFEC1 (epg) avNEM1 (epg) CPS PLEUR CWT (kg) CBUTT (cm) CGRM (mm)
Final models
N
Mean ± SD
Range
RSD
Fixed effects c
Random
4881 11,043 8989 3766 3766 11,050 9687 10,933 7821 9048
4.89 ± 0.95 30.29 ± 5.62 42.93 ± 6.19 702 ± 778 36 ± 61 0.37 ± 0.62 0.05 ± 0.22 18.2 ± 2.98 64.7 ± 3.3 5.4 ± 3.3
1.6 − 9.1 10 − 56 24.6 − 70.5 0 − 12450 0 − 550 0−2 0−1 8.6 − 33.5 52 − 79 0 − 30
0.59 3.09 3.14 0.58 0.52 0.76 1.00 1.72 1.28 1.53
CGweaning, bdev, brr, aod CGweaning, bdev, brr, aod CGkill, bdev, brr, aod CGFEC, bdev, brr, aod CGFEC, bdev, brr, aod CGkill CGkill CGkill, bdev, brr, aod CGkill, bdev, brr, aod CGkill, bdev, brr, aod
Animal, maternal Animal, maternal Animal Animal, permanent environmental Animal, permanent environmental Animal Animal Animal Animal Animal
a
N: number of observations; SD: standard deviation; RSD: residual standard deviation of transformed trait. BWT: birth weight; WWT: weaning weight; PRESLTWT: pre-slaughter liveweight; avFEC1: average summer strongyle faecal egg count; avNEM1: average summer Nematodirus faecal egg count; CPS: consolidated pneumonia score; PLEUR: pleurisy; CWT: carcass weight; CBUTT: carcass butt circumference; CGRM: depth of tissue 110 mm off the mid line in the region of the 12th rib. c CGweaning: weaning contemporary group (sex, birth year, flock, and weaning mob); bdev: birth date deviation; brr: birth rearing rank; aod: age of dam as linear and quadratic; CGFEC: FEC mob contemporary group (sex, birth year, flock, WWT mob and FEC mob); CGkill: kill contemporary group (sex, birth year, flock, weaning mob and kill date). b
Fig. 2. Incidence of pneumonia and pleurisy by flock and year of birth. a CPS: Consolidated Pneumonia Score, where 0 = no lesions present; 1 = individual lobes with up to 50% of the lobe affected and 2 = individual lobes with greater than 50% of the lobe affected. b Pleurisy data was unavailable for animals born in 2009 in flock H and I.
Table 2 Least squares means (±standard error) of weight gain (g/day) and carcass weight (CWT), classified by unadjusted Consolidated Pneumonia Score (CPS).
CPS
P-value abc
0 1 2
Birth to weaning (g/day)
Weaning to pre-slaughter (g/day)
Birth to pre-slaughter (g/day)
CWT (kg)
280.3 ± 2.0a 285.3 ± 2.2b 289.1 ± 2.7b <0.001
164.8 ± 1.7a 161.4 ± 1.9b 148.8 ± 2.3c <0.001
219.7 ± 1.2a 220.2 ± 1.3a 215.6 ± 1.6b 0.001
18.1 ± 0.1a 18.0 ± 0.1a 17.8 ± 0.2b <0.001
superscripts within column are different (P < 0.05) from each other.
observed in Southland lambs by Goodwin et al. (2004), however, that study only examined animals over one season. The incidence of pneumonic lesions varied between years, with the highest percentages observed in 2010-born lambs. This is likely to be due to a severe storm causing heavy snow during September (lambing) that resulted in large stock losses to farmers throughout the South-
land region. Exposure to cold rain or snow is a known risk factor for pneumonia (West et al., 2009). While prevalence of pneumonia has been shown to vary among regions, increasing on farms in the North Island of New Zealand, (Alley, 2002; Goodwin et al., 2004), the animals in this study were primarily from Southland-based flocks, and therefore no inferences about regional differences can be made.
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Table 3 Heritability of traits (diagonal), and genetic (below diagonal) and phenotypic (above diagonal) correlations between consolidated pneumonia score and other production traits (±standard error). Trait a
CPSa
PLEURa
BWT
WWT
PRESLTWT
FEC1
NEM1
CWT
CBUTT
CGRM
CPSa PLEURa BWT WWT PRESLTWT FEC1 NEM1 CWT CBUTT CGRM
0.07 ± 0.02 0.40 ± 0.21 0.08 ± 0.21 0.28 ± 0.20 0.35 ± 0.18 0.30 ± 0.13 0.14 ± 0.13 0.20 ± 0.18 0.22 ± 0.17 −0.10 ± 0.18
0.12 ± 0.01 0.02 ± 0.01 −0.46 ± 0.24 0.28 ± 0.28 0.12 ± 0.25 −0.03 ± 0.18 0.14 ± 0.18 −0.18 ± 0.22 0.33 ± 0.23 −0.01 ± 0.23
0.02 ± 0.02 −0.01 ± 0.02 0.24 ± 0.04 0.48 ± 0.1 0.54 ± 0.08 0.07 ± 0.07 0.13 ± 0.07 0.35 ± 0.09 0.31 ± 0.09 0.01 ± 0.10
0.07 ± 0.01 0.04 ± 0.02 0.37 ± 0.01 0.17 ± 0.03 0.87 ± 0.03 0.28 ± 0.08 0.01 ± 0.08 0.75 ± 0.06 0.73 ± 0.05 0.26 ± 0.10
−0.02 ± 0.02 −0.02 ± 0.02 0.31 ± 0.02 0.74 ± 0.01 0.35 ± 0.04 0.24 ± 0.06 0.22 ± 0.06 0.85 ± 0.03 0.75 ± 0.04 0.34 ± 0.08
0.07 ± 0.02 0.01 ± 0.02 0.01 ± 0.02 0.06 ± 0.02 0.06 ± 0.02 0.40 ± 0.04 0.28 ± 0.03 0.13 ± 0.06 0.07 ± 0.05 −0.11 ± 0.06
0.00 ± 0.02 0.01 ± 0.02 0.06 ± 0.02 −0.02 ± 0.02 0.05 ± 0.02 0.18 ± 0.02 0.37 ± 0.04 0.21 ± 0.06 0.18 ± 0.06 0.15 ± 0.06
−0.02 ± 0.02 −0.08 ± 0.02 0.21 ± 0.02 0.63 ± 0.01 0.82 ± 0.01 0.02 ± 0.02 0.05 ± 0.02 0.40 ± 0.04 0.91 ± 0.02 0.56 ± 0.06
−0.02 ± 0.02 0.01 ± 0.02 0.21 ± 0.02 0.63 ± 0.01 0.76 ± 0.01 0.01 ± 0.02 0.07 ± 0.02 0.79 ± 0.01 0.31 ± 0.04 0.33 ± 0.07
−0.06 ± 0.02 −0.07 ± 0.02 −0.03 ± 0.02 0.21 ± 0.02 0.42 ± 0.02 −0.06 ± 0.02 0.02 ± 0.02 0.50 ± 0.01 0.38 ± 0.02 0.39 ± 0.04
Repeatability
–
–
–
–
–
0.54 ± 0.02
0.52 ± 0.02
–
–
–
a
CPSa: Consolidated pneumonia score adjusted for incidence rate; PLEURa: pleurisy adjusted for incidence rate; BWT: birth weight; WWT: weaning weight; PRESLTWT: pre-slaughter liveweight; FEC1: summer strongyle faecal egg count; NEM1: summer Nematodirus faecal egg count; CWT: carcass weight; CBUTT: carcass butt circumference; CGRM: depth of tissue 110 mm off the mid line in the region of the 12th rib.
This study builds on the work of Baird et al. (2012) to provide a heritability estimate for pneumonic lesions in New Zealand mixed breed progeny tested lambs of 0.07 ± 0.02. This is consistent with the estimated heritability in the previous study (0.12 ± 0.06), which was calculated using lung scores from only 1253 animals. This heritability may incorporate breed differences as well as within breed variation. The New Zealand industry often uses mixed breed seedstock and so is able to utilise both sources of variation. While there are no other published estimates of the heritability of pneumonia in sheep, our estimate is consistent with estimates of the heritability of bovine respiratory disease (BRD) in cattle, which range from 0.04 to 0.26 (Snowder et al., 2006; Schneider et al., 2010). Genetics have been shown to play a role in the variation in host resistance for multiple diseases in livestock, including parasitic, metabolic and bacterial diseases, with the heritability ranging from moderate to low (Bishop and Morris, 2007; Berry et al., 2011). Selection using phenotypic markers for disease requires exposure to pathogens or environmental stressors, and in the case of pneumonia, slaughter for an accurate phenotype. The use of genomic tools to implement selection against susceptibility to pneumonia is an efficient alternative approach (Goddard, 2012). It is especially valuable where sires are already routinely genotyped by industry. However, to implement genomic selection a training population of related individuals with genotypes and phenotypes is required. This would be aided by routine recording of pneumonia in lungs at slaughter by processing plants. The significant positive genetic correlation observed between CPSa and FEC1 was moderate (0.30 ± 0.13), suggesting that progress in selecting for resistance to both disease traits would be easier than with no genetic correlation. If selecting for reduced FEC1, the correlated response in CPSa would be ∼70% of that which would be expected if directly selecting on CPSa (Falconer and Mackay, 1996). Although animals with FEC measurements were primarily from one flock, the implication of this genetic correlation is important for the industry and warrants further investigation. Recording of pneumonic lesions at slaughter from multiple flocks with recorded FEC measurements would extend this study to further investigate genetic correlation between FEC and CPSa. While there was no significant genetic correlation between CPSa and PLEURa, it is commonly accepted that pneumonia and pleurisy are part of a complex of poorly defined aetiology (McGowan et al., 1978; Pfeffer, 1986) and this is supported by a positive, albeit non-significant, estimate of the genetic correlation. The small numbers of animals that had either severe pneumonic lesions (CPS = 2, 7%) or pleurisy (6%) may not be enough to provide accurate estimates of the correlation between the two traits. The genetic correlation between gastrointestinal nematode resistance and productivity has been shown to be dependent on the level of infection, with the rela-
tionship strengthening as disease incidence increases (Bishop & Stear 1999). A more accurate estimation of genetic parameters would therefore require more data from flocks with a high incidence of both severe pneumonia and pleurisy. While neither CPSa nor PLEURa were significantly genetically correlated with any other measured trait, the correlations for these traits had large standard errors, which may also be aided by more records from flocks. However, low correlations between disease and production traits was also observed in a study by Pickering et al. (2012). This study found low genotypic correlations between FEC or dagginess (the accumulation of faecal material around the perineum region of sheep) and production traits, including liveweights. Heritabilities and correlations between production traits in this study were slightly higher than those previously reported in New Zealand sheep (Pickering et al., 2012; Brito et al., 2015). As these two studies consisted of a superset of the animals involved in this work they are likely more representative of the New Zealand industry as a whole. There are few studies that have examined the effect of pneumonic lesions on growth rates in lambs in a commercial situation. Two studies in which pneumonia was experimentally induced showed reduced liveweight gain in the infected lambs compared to controls (Jones et al., 1982; Alley, 1987), however, these are unlikely to reflect conditions on commercial farms. This study found that lambs with pneumonic lesions at slaughter had grown faster from birth to weaning, and then more slowly from weaning to slaughter than animals without lesions. Kirton et al. (1976) also observed that lambs subsequently diagnosed as having moderate or severe pneumonia tended to gain more weight from birth to weaning, and less weight from weaning to slaughter, than the remaining lambs, suggesting that faster growing lambs are more susceptible to pneumonia. While the authors also found that slightly heavier-than-average lambs had more extensive pneumonia, after adjusting for weaning weight, lambs with moderate to severe pneumonia had reduced final liveweight and carcass weight. Despite the reduction of 0.45 kg/lamb carcass, on average only 6.5% of lambs had moderate to severe pneumonia over the 5 year course of the experiment, and the authors concluded pneumonia was of little economic importance (Kirton et al., 1976). Goodwin et al. (2004) examined the lungs of lambs from commercial farms in Southland, the King Country, and Northland, and found reduced daily weight gain in the month before slaughter in lambs for which more than 20% of the lung surface area was affected (3.7% of animals). Animals with a CPS of 2 grew approximately 16 g/day more slowly than their counterparts with no lesions, which is considerably lower than the reduction from 136 to 65 g/day observed by Goodwin et al. (2004) in lambs with moderate to severe pneumonia. There are many contributing factors to the differences observed between studies, including different types, timing and levels of exposure to infec-
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tious agents, natural infection versus inoculation, varying scoring systems, timing of slaughter and weight measurements, as well as the location of the flocks studied and differing farm management practises. 5. Conclusions This study has shown that there is a heritable, albeit low, component to pneumonia in New Zealand sheep. Pneumonic lesion score was associated with fast growth from birth to weaning, and reduced growth between weaning and slaughter. Continued recording of the trait allowing further studies into the relationship between pneumonia and lamb growth is required. Including more data from pedigree-recorded flocks with a high incidence of severe pneumonia and pleurisy will enable more accurate estimates of genetic parameters, and subsequent correlations with production and disease traits. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements This work was supported by Beef and Lamb New Zealand Genetics, Ovita and AgResearch Core funding. The flocks involved in this study were from Beef and Lamb New Zealand Genetics (via Ovita), FarmIQ, Focus Genetics, New Zealand Perendale and Headwaters New Zealand funded progeny test programs. The authors would like to acknowledge the AgResearch Animal Genomics field staff, Hamish Bielski, Alliance Group Limited staff from the Mataura, Lorneville and Pukeuri processing plants, and Silver Fern Farms staff from the Takapau and Finegand processing plants for their help in data collection. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.smallrumres. 2016.11.003. References Alley, M.R., 1987. The effect of chronic non-progressive pneumonia on weight gain of pasturefed lambs. N. Z. Vet. J. 35, 163–166. Alley, M.R., 2002. Pneumonia in sheep in New Zealand: an overview. N. Z. Vet. J. 50, 99–101. Baird, H.J., Clarke, S.M., Johnson, P.L., 2012. BRIEF COMMUNICATION: development of a visual scoring system for ovine pneumonia at the processing plant. Proc. N. Z. Soc. Anim. Prod., 169–171.
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Berry, D.P., Bermingham, M.L., Good, M., More, S.J., 2011. Genetics of animal health and disease in cattle. Ir. Vet. J. 64, 5. Bishop, S.C., Morris, C.A., 2007. Genetics of disease resistance in sheep and goats. Small Rumin. Res. 70, 48–59. Brito, L.F., Miller, S.P., Clarke, S.M., Dodds, K.G., Bain, W.E., Lee, M.A., Pickering, N.K., McEwan, J.C., 2015. BRIEF COMMUNICATION: genetic parameters for growth, carcass and meat quality traits in New Zealand sheep. Proc. N. Z. Soc. Anim. Prod., 94–96. Brown, D.J., Atkins, K., Huisman, A.E., 2005. Expression of body weight, fleece weight and fibre diameter in across flock genetic evaluation. Proc. Assoc. Advmt. Anim. Breed. Genet., 84–87. Falconer, D.S., Mackay, T.F.C., 1996. Introduction to Quantitative Genetics, fourth ed. Longman Harlow, Essex, England. Gilmour, A.R., Gogel, B.J., Cullis, B.R., Thompson, R., 2009. ASReml User Guide Release 3.0. VSN International Ltd., Hemel Hempstead, Hertfordshire, UK. Goddard, M.E., 2012. Uses of genomics in livestock agriculture. Anim. Prod. Sci. 52, 73–77. Goodwin, K.A., Jackson, R., Brown, C., Davies, P.R., Morris, R.S., Perkins, N.R., 2004. Pneumonic lesions in lambs in New Zealand: patterns of prevalence and effects on production. N. Z. Vet. J. 52, 175–179. Goodwin-Ray, K.A., Stevenson, M., Heuer, C., 2008a. Flock-level case–control study of slaughter-lamb pneumonia in New Zealand. Prev. Vet. Med. 85, 136–149. Goodwin-Ray, K.A., Stevenson, M.A., Heuer, C., 2008b. Effect of vaccinating lambs against pneumonic pasteurellosis under New Zealand field conditions on their weight gain and pneumonic lung lesions at slaughter. Vet. Rec. 162, 9–11. Goodwin-Ray, K.A., Stevenson, M.A., Heuer, C., Cogger, N., 2008c. Economic effect of pneumonia and pleurisy in lambs in New Zealand. N. Z. Vet. J. 56, 107–114. Jones, G.E., Field, A.C., Gilmour, J.S., Rae, A.G., Nettleton, P.F., McLauchlan, M., 1982. Effects of experimental chronic pneumonia on bodyweight, feed intake and carcase composition of lambs. Vet. Rec. 110, 168–173. Kirton, A.H., O’Hara, P.J., Shortridge, E.H., Cordes, D.O., 1976. Seasonal incidence of enzootic pneumonia and its effect on the growth of lambs. N. Z. Vet. J. 24, 59–64. McGowan, B., Thurley, D.C., McSporran, K.D., Pfeffer, A.T., 1978. Enzootic pneumonia-pleurisy complex in sheep and lambs. N. Z. Vet. J. 26, 169–172. Muggli-Cockett, N.E., Cundiff, L.V., Gregory, K.E., 1992. Genetic analysis of bovine respiratory disease in beef calves during the first year of life. J. Anim. Sci. 70, 2013–2019. Pickering, N.K., Dodds, K.G., Blair, H.T., Hickson, R.E., Johnson, P.L., McEwan, J.C., 2012. Genetic parameters for production traits in New Zealand dual-purpose sheep, with an emphasis on dagginess. J. Anim. Sci. 90, 1411–1420. Pfeffer, A., 1986. The pathology and pathogenesis of pleural adhesions in sheep. N. Z. Vet. J. 34, 85–93. Schneider, M.J., Tait, R.G.J., Ruble, M.V., Busby, W.D., Reecy, J.M., 2010. Evaluation of fixed sources of variation and estimation of genetic parameters for incidence of bovine respiratory disease in preweaned calves and feedlot cattle. J. Anim. Sci. 88, 1220–1228. Snowder, G.D., Van Vleck, L.D., Cundiff, L.V., Bennett, G.L., 2005. Influence of breed, heterozygosity, and disease incidence on estimates of variance components of respiratory disease in preweaned beef calves. J. Anim. Sci. 83, 1247–1261. Snowder, G.D., Van Vleck, L.D., Cundiff, L.V., Bennett, G.L., 2006. Bovine respiratory disease in feedlot cattle: environmental, genetic, and economic factors. J. Anim. Sci. 84, 1999–2008. Stear, M.J., Bishop, S.C., Mallard, B.A., Raadsma, H.W., 2001. The sustainability, feasibility and desirability of breeding livestock for disease resistance. Res. Vet. Sci. 71, 1–7. West, D.M., Bruère, A.N., Ridler, A.L., 2009. The Sheep: Health, Disease and Production, third ed. New Zealand Veterinary Association, Wellington, NZ. Zheng, T., Gupta, S.K., McCarthy, A.R., Moffat, J., Buddle, B.M., 2015. Cross-protection study of a Mannheimia haemolytica serotype 1 vaccine against acute pasteurellosis in lambs induced by a serotype 2 strain. Vet. Microbiol. 177, 386–393.
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Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Incidence and heritability of ovine pneumonia, and the relationship with production traits in New Zealand sheep Kathryn M. McRae, Hayley J. Baird, Ken G. Dodds, Matthew J. Bixley, Shannon M. Clarke ∗ AgResearch Invermay, Private Bag 50034, Mosgiel 9053, New Zealand
a r t i c l e
i n f o
Article history: Received 28 April 2016 Received in revised form 3 August 2016 Accepted 4 November 2016 Available online 8 November 2016 Keywords: Sheep Pneumonia Heritability Disease
a b s t r a c t The cost of ovine pneumonia and pleurisy to the New Zealand economy is high, with the majority of loss through slower growth and reduced carcass value at slaughter. Farm management practices and vaccine development have traditionally been the main focus for prevention of pneumonia. The objective of this study was to estimate the heritability of pneumonia in New Zealand lambs, and investigate the genetic relationship with key production traits. The lungs of 11,437 lambs from pedigree-recorded flocks were scored for the presence and severity of pneumonic lesions at slaughter. On average 28% of lambs had pneumonic lesions at slaughter, with 7% showing severe lesions. The incidence of pleurisy in these animals was 6%. Heritability estimates for pneumonic lesions and pleurisy were 0.07 ± 0.02 and 0.02 ± 0.01, respectively. There was a significant positive genetic correlation between pneumonic lesions and faecal egg count (0.30 ± 0.13). Animals with pneumonic lesions had grown faster from birth to weaning, and slower from weaning to slaughter than animals without lesions. This study has shown that there is a heritable component to pneumonia in sheep. Including more data from pedigree-recorded flocks with severe pneumonia and a high incidence of pleurisy will enable more accurate estimates of genetic parameters, and subsequent correlations with production and disease traits. This would be aided by routine recording of pneumonia in lungs at slaughter by processing plants. © 2016 Published by Elsevier B.V.
1. Introduction Respiratory diseases, including pneumonia, are common in most livestock around the world. The economic cost of pneumonia to the New Zealand sheep industry is high and consists of three main factors; direct losses of stock on farm, reduced weight gains and wool production from sub-clinical animals, and condemnation and downgrading of carcasses at slaughter (West et al., 2009). A study by Goodwin-Ray et al. (2008c) estimated the annual cost of pneumonia to the New Zealand sheep industry to be NZD$1.36 to $3.31 per lamb, with the prevalence of pneumonia during February through April having the greatest impact on cost. However, this is a conservative estimate of the cost to the industry given the study did not include the costs associated with pneumonia related mortalities on farm. Pneumonia has been reported to have a significant effect on lamb growth rate (Kirton et al., 1976; Alley, 1987; Goodwin et al., 2004). The extent of the loss depends on the study; the first study of its kind in New Zealand sheep
∗ Corresponding author. E-mail address: [email protected] (S.M. Clarke). http://dx.doi.org/10.1016/j.smallrumres.2016.11.003 0921-4488/© 2016 Published by Elsevier B.V.
by Kirton et al. (1976) showed that when adjusted for weaning weight moderate to severe pneumonia reduced carcass weights by 450 g. Alley (1987) found that carcass weights of lambs with experimentally-induced chronic non-progressive pneumonia were on average 1.5 kg lighter than controls over a 2 month period. Goodwin et al. (2004) addressed the relationship between severity of pneumonia and average daily gain (ADG) in the month prior to slaughter, finding that when more than 20% of the lung surface area was affected by pneumonia, ADG decreased from 136 to 65 g/day. In sheep respiratory disease is etiologically complex, resulting from an interaction of the infectious agents (bacterial, mycobacterial, and viral) with the host’s defence mechanisms, which are often compromised by environmental factors (Alley, 2002). In New Zealand the term chronic non-progressive pneumonia (CNP) is typically used to describe subclinical pneumonia, which is widespread among lambs (Goodwin et al., 2004). Acute pneumonia occurs more sporadically, and occurs in sheep of all ages. The disease has a rapid onset and the first sign is often the death of the affected animal, although recovery with chronic lesions may also occur (Alley, 2002). Animals that have subclinical pneumonia and those that have survived clinical pneumonia may develop pleurisy, where the lungs adhere to the chest wall.
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Clinical diagnosis of pneumonia is difficult, with accurate diagnosis requiring post-mortem examination of the lungs; hence the animal needs to be euthanised. Traditionally, the main focus for prevention of pneumonia has been farm management practices and vaccine development. A case-control study by Goodwin-Ray et al. (2008a) identified shearing lambs at weaning, breeding replacement ewes on farm and contact with other flocks through the purchase of lambs post-weaning as practises likely to increase pneumonia prevalence. Vitamin B12 treatments at time of docking and weaning, as well as set stocking lambs post-weaning, were seen as protective practises. Lambs slaughtered later in the season versus at or around the time of weaning are at much higher risk, but this is more likely to be a consequence of slower growth because of pneumonia than a cause of pneumonia. A vaccine based on the serotype S1 strain of Mannheimia haemolytica, the primary cause of lung damage, has been shown to provide cross-protection against S2 strains in an experimental challenge (Zheng et al., 2015). The evaluation of a commercial vaccine containing antigens of M. haemolytica and Pasteurella trehalosi (Ovipast Plus, Intervet) under field conditions showed no difference in prevalence of pneumonic lesions or ADG between the placebo-treated and vaccinated lambs (Goodwin-Ray et al., 2008b). Improvement of animal health through genetic selection can provide a complementary approach to disease control (Stear et al., 2001; Bishop and Morris, 2007; Berry et al., 2011). Baird et al. (2012) developed a pneumonic lesion scoring system in the processing plant (chain speed), and estimated the heritability of the consolidated pneumonic lesion score in pedigree-recorded lambs to be 0.12 ± 0.06. This is comparable to estimates of heritability of bovine respiratory disease (BRD) resistance in cattle, which range from 0.04 to 0.26 (Muggli-Cockett et al., 1992; Snowder et al., 2005; Schneider et al., 2010). The objective of this study was to expand on previous work to estimate the heritability of pneumonic lesions in New Zealand lambs, and, in addition, investigate the genetic relationship with key production traits
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lungs were fresh. For lambs born 2008–2010 this was determined by removing the lungs from the processing chain and visually assessing each of the five lobes. Each lobe was scored on a 0–5 scale, indicating the percentage of surface area affected, where 0 = no lesions present; 1 = small lesions; 2 = approximately 25% of the lobe affected; 3 = approximately 50% of the lobe affected; 4 = approximately 75% of the lobe affected and 5 = 100% of the lobe affected. Pneumonic lesions were defined as compacted, dark purple-red areas of the lung that were firm to touch (Fig. 1B and C). The sum of the individual lobe scores was calculated and recorded as a ‘total lesion score’ (TLS). The TLS system is not appropriate for recording pneumonic lesions at chain-speed on the processing chain at the plant, where up to 10 animals per minute may be slaughtered. A refined scoring system was devised by Baird et al. (2012) and was implemented for recording pneumonic lesions at chain-speed from the progeny born in 2011 onwards. This refined TLS system, termed ‘consolidated pneumonia score’ (CPS), has a range from 0 to 2, where 0 = no lesions present; 1 = any individual lobe with up to 50% of the lobe affected and 2 = any individual lobe with greater than 50% of the lobe affected (Fig. 1). Animals that had been scored under the TLS system were retrospectively given CPS values, and CPS was used for all subsequent analysis. 2.3. Production Traits Carcass weight (CWT), and primary and secondary carcass fault data, including pleurisy (PLEUR) were obtained from the meat processing plant. The carcass measurements of depth of tissue 110 mm off the mid line in the region of the 12th rib (CGRM) and carcass butt circumference (CBUTT) were measured the day post-slaughter, before the further processing of the carcass. All other data, including Julian date of birth (JDOB), birth rearing rank (BRR; born as a single, twin or triplet, and raised as a single, twin or triplet), age of dam AOD; (1 year old, 2 years old, or older), birth weight (BWT), weaning weight (WWT), weaning weight mob, pre-slaughter weight (PRESLTWT), pedigree, date of slaughter and breed were obtained from Sheep Improvement Limited (SIL) records.
2. Materials and methods 2.4. Statistical analysis The work reported here was undertaken using records sourced from New Zealand sheep breeders and stored in the Sheep Improvement Limited database (SIL, www.sil.co.nz). The animals were managed in accordance with the provisions of the New Zealand Animal Welfare Act 1999, and the New Zealand Codes of Welfare developed under sections 68–79 of the Act. 2.1. Animals The lungs from a total of 11,437 ram and ewe lambs from one North Island (Flock H) and eight (Flocks A–G and I) Southland and Otago pedigree-recorded flocks were scored for the presence and severity of pneumonic lesions. Data collection was carried out from January to May. Animals from flocks I and E were selected for slaughter by weight and body condition score at 3 different time points. Pneumonic lesions were only recorded in lambs slaughtered at the second and third time points, as preliminary studies had shown little to no lesions in the lungs of lambs slaughtered at weaning. All other flocks were fixed-date slaughters, and primarily took place between February and March. Animals were predominantly composites of the main dual-purpose sheep breeds used in New Zealand, including Romney, Coopworth, Perendale, and Texel. 2.2. Pneumonia scoring system The extent of the pneumonic lesions within the lungs was determined post-slaughter at the processing plant, ensuring the
Data cleaning consisted of removal of records with 1) missing values for sire information or weaning weight, and 2) contemporary groups containing less than 5 observations. Weight and slaughter traits were adjusted using SIL standard practice (S-A. Newman, personal communication) to account for relationships between contemporary group mean and variance, using the equation: aTr = (Tr/Trm)*oTrm where Trm is the mean for the contemporary group, and oTrm is the overall mean for the trait (Brown et al., 2005). Contemporary group (CG) was specific to each trait, and was defined as flock, birth year, sex, weaning mob and trait/slaughter mob combination. The traits adjusted using this approach were BWT, WWT, PRESLTWT, CWT, CBUTT and CGRM. Summer faecal egg count values are a repeatable trait, and were estimated from two samples, taken several days apart. These were distinguished as Nematodirus (NEM1) or ‘other trichostrongyles’ (FEC1; primarily Teladorsagia spp, Trichostrongylus spp and Cooperia curticei). Both FEC1 and NEM1 values were log transformed before analysis (ln(X + 25)). To account for lack of challenge in some contemporary groups (CGkill; sex, birth year, flock, weaning mob and kill date), data was set to missing if the mean CPS in that contemporary group was below 0.1. This is assuming that animals in the contemporary groups where CPS was low were not sufficiently exposed to stressors and pathogens to express a phenotype. To adjust for heteroscedasticity, CPS (initially scored as 0, 1 or 2) was scaled using the formula CPSa = CPS/SQRT(CPSm*(2-CPSm)), where m is the
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Fig. 1. Consolidated pneumonia score (CPS) scoring system. Pneumonic lesions were defined as compacted areas of the lung that are dark purple-red in appearance, and firm to touch (examples shown by arrows). Lungs were scored as 0 = no lesions present (A); 1 = any individual lobe with up to 50% of the lobe affected (B) or 2 = any individual lobe with greater than 50% of the lobe affected (C).
incidence rate per contemporary group (CGkill). Pleurisy (initially coded as 0 or 1) values were also transformed using the formula PLEURa = PLEUR/SQRT(PLEURm*(1-PLEURm)). Data analysis models were determined for each trait separately using forward and backward selection in R. Model selection and comparison was conducted using the Bayesian Information Criterion (BIC) and R2 . Fixed effects fitted included trait contemporary group, birth-rearing rank, and age of dam fitted as linear (AOD) and quadratic (AOD2 ) effects. Birthday deviation (BDEV) from the mean of the contemporary group (CGweaning: sex, flock, year and weaning mob) was calculated using JDOB and fitted as a covariate. The final dataset used in the analysis contained records for 11,409 lambs, and the final models are presented in Table 1. The relationship between growth rates and untransformed CPS was examined using the GLM procedure in SAS (SAS Institute Inc., Cary NC, USA), additionally fitting BDEV, BRR, AOD and contemporary group in the model. Variance and covariance components were estimated using restricted maximum likelihood (REML) procedures fitting an animal model in ASReml (Gilmour et al., 2009), with maternal and permanent environmental effects fitted when appropriate (Table 1). Heritabilities were obtained from univariate analyses of the respective traits, and genotypic and phenotypic correlations between traits were obtained from bivariate analyses.
3.2. The effect of pneumonia on growth and carcass weight Table 2 shows the least squares means (± standard error) of growth rates and CWT classified by CPS. Animals with pneumonic lesions (CPS > 0) at slaughter had grown faster from birth to weaning (P < 0.001), and slower from weaning to pre-slaughter (P < 0.01) than animals without lesions. There was no difference in growth rate between animals scored as 1 or 2 from birth to weaning, however animals with a CPS of 2 grew more slowly than animals with a CPS of 1 from weaning to slaughter (P < 0.001). Animals with more than 50% of a lobe affected by pneumonic lesions (CPS = 2) grew more slowly from birth to slaughter and had a lower carcass weight than both those with less than 50% affected (CPS = 1) or no pneumonic lesions (CPS = 0; P < 0.01). 3.3. Genetic parameters Heritabilities and correlations are presented in Table 3. The heritability estimates for CPSa and PLEURa were 0.07 ± 0.02 and 0.02 ± 0.01, respectively. The genetic correlation between CPSa and FEC1 was significant and positive (0.30 ± 0.13). Neither CPSa nor PLEURa were significantly genetically correlated with any other measured trait, including liveweights or carcass measurements.
3. Results
4. Discussion
3.1. Incidence of pneumonia and pleurisy
Investigation of the genetic relationships underlying complex traits such as pneumonia requires the collection of prevalence data from a large number of pedigree recorded flocks. The development of a visual scoring system of lungs for pneumonic lesions that can be implemented at the processing plant (Baird et al., 2012) was utilised to examine the incidence of pneumonic lesions at slaughter, and the effects on production traits. The average incidence over all of the years measured was 28%. This is higher than the 21.8%
The incidence of pneumonic lesions and pleurisy was recorded for 11,471 lambs born between 2008 and 2014 (Fig. 2 and Supplementary Table 1). The overall incidence of pneumonic lesions (CPS of 1 or 2) was 28% (range 9%–52% over cohorts), with an average of 7% (range 0%–18%) of animals having a score of 2. The incidence of pleurisy in these animals was 6% (range 0%–16%).
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Table 1 Descriptive unadjusted statistics and final mixed models used for individual trait analysis. Descriptive analysis a Trait
b
BWT (kg) WWT (kg) PRESLTWT (kg) avFEC1 (epg) avNEM1 (epg) CPS PLEUR CWT (kg) CBUTT (cm) CGRM (mm)
Final models
N
Mean ± SD
Range
RSD
Fixed effects c
Random
4881 11,043 8989 3766 3766 11,050 9687 10,933 7821 9048
4.89 ± 0.95 30.29 ± 5.62 42.93 ± 6.19 702 ± 778 36 ± 61 0.37 ± 0.62 0.05 ± 0.22 18.2 ± 2.98 64.7 ± 3.3 5.4 ± 3.3
1.6 − 9.1 10 − 56 24.6 − 70.5 0 − 12450 0 − 550 0−2 0−1 8.6 − 33.5 52 − 79 0 − 30
0.59 3.09 3.14 0.58 0.52 0.76 1.00 1.72 1.28 1.53
CGweaning, bdev, brr, aod CGweaning, bdev, brr, aod CGkill, bdev, brr, aod CGFEC, bdev, brr, aod CGFEC, bdev, brr, aod CGkill CGkill CGkill, bdev, brr, aod CGkill, bdev, brr, aod CGkill, bdev, brr, aod
Animal, maternal Animal, maternal Animal Animal, permanent environmental Animal, permanent environmental Animal Animal Animal Animal Animal
a
N: number of observations; SD: standard deviation; RSD: residual standard deviation of transformed trait. BWT: birth weight; WWT: weaning weight; PRESLTWT: pre-slaughter liveweight; avFEC1: average summer strongyle faecal egg count; avNEM1: average summer Nematodirus faecal egg count; CPS: consolidated pneumonia score; PLEUR: pleurisy; CWT: carcass weight; CBUTT: carcass butt circumference; CGRM: depth of tissue 110 mm off the mid line in the region of the 12th rib. c CGweaning: weaning contemporary group (sex, birth year, flock, and weaning mob); bdev: birth date deviation; brr: birth rearing rank; aod: age of dam as linear and quadratic; CGFEC: FEC mob contemporary group (sex, birth year, flock, WWT mob and FEC mob); CGkill: kill contemporary group (sex, birth year, flock, weaning mob and kill date). b
Fig. 2. Incidence of pneumonia and pleurisy by flock and year of birth. a CPS: Consolidated Pneumonia Score, where 0 = no lesions present; 1 = individual lobes with up to 50% of the lobe affected and 2 = individual lobes with greater than 50% of the lobe affected. b Pleurisy data was unavailable for animals born in 2009 in flock H and I.
Table 2 Least squares means (±standard error) of weight gain (g/day) and carcass weight (CWT), classified by unadjusted Consolidated Pneumonia Score (CPS).
CPS
P-value abc
0 1 2
Birth to weaning (g/day)
Weaning to pre-slaughter (g/day)
Birth to pre-slaughter (g/day)
CWT (kg)
280.3 ± 2.0a 285.3 ± 2.2b 289.1 ± 2.7b <0.001
164.8 ± 1.7a 161.4 ± 1.9b 148.8 ± 2.3c <0.001
219.7 ± 1.2a 220.2 ± 1.3a 215.6 ± 1.6b 0.001
18.1 ± 0.1a 18.0 ± 0.1a 17.8 ± 0.2b <0.001
superscripts within column are different (P < 0.05) from each other.
observed in Southland lambs by Goodwin et al. (2004), however, that study only examined animals over one season. The incidence of pneumonic lesions varied between years, with the highest percentages observed in 2010-born lambs. This is likely to be due to a severe storm causing heavy snow during September (lambing) that resulted in large stock losses to farmers throughout the South-
land region. Exposure to cold rain or snow is a known risk factor for pneumonia (West et al., 2009). While prevalence of pneumonia has been shown to vary among regions, increasing on farms in the North Island of New Zealand, (Alley, 2002; Goodwin et al., 2004), the animals in this study were primarily from Southland-based flocks, and therefore no inferences about regional differences can be made.
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Table 3 Heritability of traits (diagonal), and genetic (below diagonal) and phenotypic (above diagonal) correlations between consolidated pneumonia score and other production traits (±standard error). Trait a
CPSa
PLEURa
BWT
WWT
PRESLTWT
FEC1
NEM1
CWT
CBUTT
CGRM
CPSa PLEURa BWT WWT PRESLTWT FEC1 NEM1 CWT CBUTT CGRM
0.07 ± 0.02 0.40 ± 0.21 0.08 ± 0.21 0.28 ± 0.20 0.35 ± 0.18 0.30 ± 0.13 0.14 ± 0.13 0.20 ± 0.18 0.22 ± 0.17 −0.10 ± 0.18
0.12 ± 0.01 0.02 ± 0.01 −0.46 ± 0.24 0.28 ± 0.28 0.12 ± 0.25 −0.03 ± 0.18 0.14 ± 0.18 −0.18 ± 0.22 0.33 ± 0.23 −0.01 ± 0.23
0.02 ± 0.02 −0.01 ± 0.02 0.24 ± 0.04 0.48 ± 0.1 0.54 ± 0.08 0.07 ± 0.07 0.13 ± 0.07 0.35 ± 0.09 0.31 ± 0.09 0.01 ± 0.10
0.07 ± 0.01 0.04 ± 0.02 0.37 ± 0.01 0.17 ± 0.03 0.87 ± 0.03 0.28 ± 0.08 0.01 ± 0.08 0.75 ± 0.06 0.73 ± 0.05 0.26 ± 0.10
−0.02 ± 0.02 −0.02 ± 0.02 0.31 ± 0.02 0.74 ± 0.01 0.35 ± 0.04 0.24 ± 0.06 0.22 ± 0.06 0.85 ± 0.03 0.75 ± 0.04 0.34 ± 0.08
0.07 ± 0.02 0.01 ± 0.02 0.01 ± 0.02 0.06 ± 0.02 0.06 ± 0.02 0.40 ± 0.04 0.28 ± 0.03 0.13 ± 0.06 0.07 ± 0.05 −0.11 ± 0.06
0.00 ± 0.02 0.01 ± 0.02 0.06 ± 0.02 −0.02 ± 0.02 0.05 ± 0.02 0.18 ± 0.02 0.37 ± 0.04 0.21 ± 0.06 0.18 ± 0.06 0.15 ± 0.06
−0.02 ± 0.02 −0.08 ± 0.02 0.21 ± 0.02 0.63 ± 0.01 0.82 ± 0.01 0.02 ± 0.02 0.05 ± 0.02 0.40 ± 0.04 0.91 ± 0.02 0.56 ± 0.06
−0.02 ± 0.02 0.01 ± 0.02 0.21 ± 0.02 0.63 ± 0.01 0.76 ± 0.01 0.01 ± 0.02 0.07 ± 0.02 0.79 ± 0.01 0.31 ± 0.04 0.33 ± 0.07
−0.06 ± 0.02 −0.07 ± 0.02 −0.03 ± 0.02 0.21 ± 0.02 0.42 ± 0.02 −0.06 ± 0.02 0.02 ± 0.02 0.50 ± 0.01 0.38 ± 0.02 0.39 ± 0.04
Repeatability
–
–
–
–
–
0.54 ± 0.02
0.52 ± 0.02
–
–
–
a
CPSa: Consolidated pneumonia score adjusted for incidence rate; PLEURa: pleurisy adjusted for incidence rate; BWT: birth weight; WWT: weaning weight; PRESLTWT: pre-slaughter liveweight; FEC1: summer strongyle faecal egg count; NEM1: summer Nematodirus faecal egg count; CWT: carcass weight; CBUTT: carcass butt circumference; CGRM: depth of tissue 110 mm off the mid line in the region of the 12th rib.
This study builds on the work of Baird et al. (2012) to provide a heritability estimate for pneumonic lesions in New Zealand mixed breed progeny tested lambs of 0.07 ± 0.02. This is consistent with the estimated heritability in the previous study (0.12 ± 0.06), which was calculated using lung scores from only 1253 animals. This heritability may incorporate breed differences as well as within breed variation. The New Zealand industry often uses mixed breed seedstock and so is able to utilise both sources of variation. While there are no other published estimates of the heritability of pneumonia in sheep, our estimate is consistent with estimates of the heritability of bovine respiratory disease (BRD) in cattle, which range from 0.04 to 0.26 (Snowder et al., 2006; Schneider et al., 2010). Genetics have been shown to play a role in the variation in host resistance for multiple diseases in livestock, including parasitic, metabolic and bacterial diseases, with the heritability ranging from moderate to low (Bishop and Morris, 2007; Berry et al., 2011). Selection using phenotypic markers for disease requires exposure to pathogens or environmental stressors, and in the case of pneumonia, slaughter for an accurate phenotype. The use of genomic tools to implement selection against susceptibility to pneumonia is an efficient alternative approach (Goddard, 2012). It is especially valuable where sires are already routinely genotyped by industry. However, to implement genomic selection a training population of related individuals with genotypes and phenotypes is required. This would be aided by routine recording of pneumonia in lungs at slaughter by processing plants. The significant positive genetic correlation observed between CPSa and FEC1 was moderate (0.30 ± 0.13), suggesting that progress in selecting for resistance to both disease traits would be easier than with no genetic correlation. If selecting for reduced FEC1, the correlated response in CPSa would be ∼70% of that which would be expected if directly selecting on CPSa (Falconer and Mackay, 1996). Although animals with FEC measurements were primarily from one flock, the implication of this genetic correlation is important for the industry and warrants further investigation. Recording of pneumonic lesions at slaughter from multiple flocks with recorded FEC measurements would extend this study to further investigate genetic correlation between FEC and CPSa. While there was no significant genetic correlation between CPSa and PLEURa, it is commonly accepted that pneumonia and pleurisy are part of a complex of poorly defined aetiology (McGowan et al., 1978; Pfeffer, 1986) and this is supported by a positive, albeit non-significant, estimate of the genetic correlation. The small numbers of animals that had either severe pneumonic lesions (CPS = 2, 7%) or pleurisy (6%) may not be enough to provide accurate estimates of the correlation between the two traits. The genetic correlation between gastrointestinal nematode resistance and productivity has been shown to be dependent on the level of infection, with the rela-
tionship strengthening as disease incidence increases (Bishop & Stear 1999). A more accurate estimation of genetic parameters would therefore require more data from flocks with a high incidence of both severe pneumonia and pleurisy. While neither CPSa nor PLEURa were significantly genetically correlated with any other measured trait, the correlations for these traits had large standard errors, which may also be aided by more records from flocks. However, low correlations between disease and production traits was also observed in a study by Pickering et al. (2012). This study found low genotypic correlations between FEC or dagginess (the accumulation of faecal material around the perineum region of sheep) and production traits, including liveweights. Heritabilities and correlations between production traits in this study were slightly higher than those previously reported in New Zealand sheep (Pickering et al., 2012; Brito et al., 2015). As these two studies consisted of a superset of the animals involved in this work they are likely more representative of the New Zealand industry as a whole. There are few studies that have examined the effect of pneumonic lesions on growth rates in lambs in a commercial situation. Two studies in which pneumonia was experimentally induced showed reduced liveweight gain in the infected lambs compared to controls (Jones et al., 1982; Alley, 1987), however, these are unlikely to reflect conditions on commercial farms. This study found that lambs with pneumonic lesions at slaughter had grown faster from birth to weaning, and then more slowly from weaning to slaughter than animals without lesions. Kirton et al. (1976) also observed that lambs subsequently diagnosed as having moderate or severe pneumonia tended to gain more weight from birth to weaning, and less weight from weaning to slaughter, than the remaining lambs, suggesting that faster growing lambs are more susceptible to pneumonia. While the authors also found that slightly heavier-than-average lambs had more extensive pneumonia, after adjusting for weaning weight, lambs with moderate to severe pneumonia had reduced final liveweight and carcass weight. Despite the reduction of 0.45 kg/lamb carcass, on average only 6.5% of lambs had moderate to severe pneumonia over the 5 year course of the experiment, and the authors concluded pneumonia was of little economic importance (Kirton et al., 1976). Goodwin et al. (2004) examined the lungs of lambs from commercial farms in Southland, the King Country, and Northland, and found reduced daily weight gain in the month before slaughter in lambs for which more than 20% of the lung surface area was affected (3.7% of animals). Animals with a CPS of 2 grew approximately 16 g/day more slowly than their counterparts with no lesions, which is considerably lower than the reduction from 136 to 65 g/day observed by Goodwin et al. (2004) in lambs with moderate to severe pneumonia. There are many contributing factors to the differences observed between studies, including different types, timing and levels of exposure to infec-
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tious agents, natural infection versus inoculation, varying scoring systems, timing of slaughter and weight measurements, as well as the location of the flocks studied and differing farm management practises. 5. Conclusions This study has shown that there is a heritable, albeit low, component to pneumonia in New Zealand sheep. Pneumonic lesion score was associated with fast growth from birth to weaning, and reduced growth between weaning and slaughter. Continued recording of the trait allowing further studies into the relationship between pneumonia and lamb growth is required. Including more data from pedigree-recorded flocks with a high incidence of severe pneumonia and pleurisy will enable more accurate estimates of genetic parameters, and subsequent correlations with production and disease traits. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements This work was supported by Beef and Lamb New Zealand Genetics, Ovita and AgResearch Core funding. The flocks involved in this study were from Beef and Lamb New Zealand Genetics (via Ovita), FarmIQ, Focus Genetics, New Zealand Perendale and Headwaters New Zealand funded progeny test programs. The authors would like to acknowledge the AgResearch Animal Genomics field staff, Hamish Bielski, Alliance Group Limited staff from the Mataura, Lorneville and Pukeuri processing plants, and Silver Fern Farms staff from the Takapau and Finegand processing plants for their help in data collection. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.smallrumres. 2016.11.003. References Alley, M.R., 1987. The effect of chronic non-progressive pneumonia on weight gain of pasturefed lambs. N. Z. Vet. J. 35, 163–166. Alley, M.R., 2002. Pneumonia in sheep in New Zealand: an overview. N. Z. Vet. J. 50, 99–101. Baird, H.J., Clarke, S.M., Johnson, P.L., 2012. BRIEF COMMUNICATION: development of a visual scoring system for ovine pneumonia at the processing plant. Proc. N. Z. Soc. Anim. Prod., 169–171.
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