Assessment of genetic variation for pathogen-specific mastitis resistance in Valle del Belice dairy sheep
- Marco Tolone†1Email author,
- Cristian Larrondo†2,
- José M. Yáñez2,
- Scott Newman3,
- Maria Teresa Sardina1 and
- Baldassare Portolano1
© The Author(s). 2016
Received: 24 October 2015
Accepted: 20 July 2016
Published: 28 July 2016
Mastitis resistance is a complex and multifactorial trait, and its expression depends on both genetic and environmental factors, including infection pressure. The objective of this research was to determine the genetic basis of mastitis resistance to specific pathogens using a repeatability threshold probit animal model.
The most prevalent isolated pathogens were coagulase-negative staphylococci (CNS); 39 % of records and 77 % of the animals infected at least one time in the whole period of study. There was significant genetic variation only for Streptococci (STR). In addition, there was a positive genetic correlation between STR and all pathogens together (ALL) (0.36 ± 0.22), and CNS and ALL (0.92 ± 0.04).
The results of our study support the presence of significant genetic variation for mastitis caused by Streptococci and suggest the importance of discriminating between different pathogens causing mastitis due to the fact that they most likely influence different genetic traits. Low heritabilities for pathogen specific-mastitis resistance may be considered when including bacteriological status as a measure of mastitis presence to implement breeding strategies for improving udder health in dairy ewes.
KeywordsEwes Mastitis Pathogen Resistance
Mastitis is one of the most common diseases affecting dairy sheep. Mastitis leads to major economic losses, mainly due to discarded milk, reduced milk production and quality, alteration of cheese-making properties, early culling, and increased health care costs [1–8]. The alterations or reductions of the dry matter of milk and its composition, have a substantial effect on the economic and industrial values of the milk, considering that almost all is processed into fermented products and cheeses [4, 9, 10]. Mastitis resistance is a complex and multifactorial trait, and its expression depends on both genetic and environmental factors, including infection pressure. In the broadest sense, resistance could be defined as the ability to avoid any infection and/or the quick recovery from an infection [11, 12], and involves different factors such as to avoid entry of the pathogen into the mammary gland, to induce an immune response capable of limiting pathogen development in the udder and to recover from the infection, as well as controlling the pathogenic effects of the infection, such as tissue damage .
Over 100 different micro-organisms can cause mastitis, in particular coliform bacteria, staphylococci and streptococci . In dairy sheep the most important agents involved in clinical mastitis are the bacterial infections, and the most frequently isolated pathogens are coagulase-negative staphylococci (CNS); that are present on and around the udder skin  with a different pathogenicity causing clinical and subclinical mastitis [15–18]. The bacterial pathogens responsible for infection of the mammary gland may be grouped into two main categories: major and minor pathogens. Major pathogen infection generally results in clinical illness or strong inflammatory responses and reduced milk yields, whereas minor pathogen infection is usually subclinical .
Selection for genetic resistance to mastitis can be done directly or indirectly. Direct selection corresponds to the diagnosis of the infection: the actual trait [i.e., bacteriological examination of milk and/or observation of clinical cases of mastitis] is measured on the animal or its relatives. Indirect selection corresponds to a prediction of the bacteriological status of the udder based on traits related to the infection [e.g., inflammatory parameters]: an indicator trait for mastitis is measured on the animal itself or its relatives . Simple and indirect methods have been widely applied based on the evaluation of the degree of inflammation or of internal mammary lesions . Their accuracy was established by bacteriological analysis as a reference method . Among the indirect methods, the most frequently used to detect mastitis are milk somatic cell count (SCC). SCC is considered as a good measure to indirectly select for mastitis resistance in cattle, especially when a direct measure of clinical mastitis incidence is not available [18, 22]. In cattle, values of SCC between 250 and 300 × 103 cells/mL are recommended as satisfactory discrimination thresholds to distinguish between healthy and infected udders. In sheep there is no widely accepted threshold [15, 23] but some studies suggested a critical limit of 500 × 103 cells/mL . There are few studies concerning genetic variation of mastitis in sheep according to bacteriological status [22, 25]. A genetic selection approach could be one of the strategies for controlling mastitis and has been shown to be a valid option, together with management, to prevent mastitis cases [1, 26]. Studies have reported genetic variation accounting for resistance to mastitis in Valle del Belice dairy sheep [22, 24]. These authors have defined mastitis as a binary trait distinguishing between ewes with at least one case of mastitis (1) and ewes without (0) in a defined period of lactation and was analyzed using a linear model approach. This definition excluded alternative definitions, for example multiple cases of mastitis within lactation, and ignored the etiology of intra-mammary infections. The purpose of this study was to determine the genetic bases of pathogen-specific resistance to mastitis in Valle del Belice dairy sheep using a threshold repeated model.
Mean, standard deviation (SD), minimum (Min) and maximum (Max) number of records per ewe within lactation
Trait definition and statistical model
Where y ijklmn is the observation for the specific pathogen causing mastitis (CNS, STR, ESCCL, STHAU, STPDG, STPUB, STPAG, BACIL, CORLT, PASCL, PSELT and ALL); Φ is the normal cumulative density function; μ is the fixed effect of the overall mean; OP i is the order of parity fitted as fixed effect (with 5 classes); MY j is the milk production yield fitted as covariate; FYS l is the flock-year-season random effect (51 classes); PE m is the random permanent environmental effect of the individual m across lactations (2350 levels with records); and A n is the random animal effect (5856 levels in the pedigree). The implicit residual variance on the underlying scale is 1 for the probit model (standard normal). Parameters of the univariate threshold models were estimated using ASREML version 3.0 .
Where σ a 2 is the animal additive genetic variance, σ FYS 2 is the variance associated with flock-year-season, σ PE 2 is the variance due to permanent environment and σ e 2 is residual variance. For all traits, the animal effect was assumed ~ N(0, A σ a 2 ), where A is the additive genetic relationship matrix among all animals included in the pedigree (5856). Similarly, FYS and PE effects were assumed ~ N(0, I σ FYS 2 ) and ~ N(0, I σ PE 2 ) , where I is an identity matrix with order equal to number of FYS and PE classes (51 and 2350) respectively.
Arithmetic mean and SD for MY, SCC, and SCS of infected and uninfected udders
SCC(x 103) a
Mean ± SD
Mean ± SD
Mean ± SD
1275 ± 544
2908 ± 4926
6.21 ± 2.45
1338 ± 558
1155 ± 3083
4.55 ± 2.13
1314 ± 553
1815 ± 3972
5.18 ± 2.33
There was a low prevalence of isolation due to CORLT, ESCCL, PASCL, PSELT, STPDG, STPUB, STPAG, and BACIL, in all the observations and according to infection status of animals. Models did not converge for these pathogens, most likely due to the low incidence (zero inflation).
Absolute (AF) and relative (RF) frequency distribution according to udder status of observations (n = 20,519)
Absolute (AF) and relative (RF) frequency distribution according to udder status of animals (n = 2350) per pathogen
Estimates of components of variance and their standard errors for infectious status
σ 2 FYS
σ 2 PE
σ a 2
σ P 2
0.79 ± 0.17
0.40 ± 0.03
0.04 ± 0.02
2.23 ± 0.17
0.02 ± 0.01
0.18 ± 0.04
0.39 ± 0.03
0.03 ± 0.02
1.60 ± 0.05
0.02 ± 0.01
0.09 ± 0.03
0.39 ± 0.07
0.15 ± 0.07
1.62 ± 0.05
0.09 ± 0.04
Phenotypic (above diagonal) and genetic (below diagonal) correlations and standard errors for resistance to mastitis
−0.08 ± 0.02
0.17 ± 0.01
0.24 ± 0.25
0.87 ± 0.01
0.36 ± 0.22
0.92 ± 0.04
The overall infection prevalence considering frequency of infection on all the samples of records was 37.7 %, close to the value of 42 % reported in a previous investigation in the same breed , and higher than the values of 26.2 and 24.6 % reported by Pengov  and Gonzalo et al. , respectively. However, in the study of Pengov  only one milk sample (n = 496 samples, 251 ewes) of udder halves was considered, whereas the study of Gonzalo et al.  was based only on subclinical mastitis prevalence. When the prevalence was assessed on all the animals it increased to 74 %, higher than any prevalence reported in previous studies.
Probably the high SCC reported in our study are a consequence of inadequate preventive management, a lack of strict hygiene conditions and extensive management practices, generating a high number of subclinical mastitis cases due to environmental pathogens. Moreover, our results suggested that ewes have higher SCC than cows and it is therefore necessary to establish an acceptable threshold in dairy sheep considering the difference in SCC between breeds and other factors [15, 18, 22].
Leitner et al.  suggested categories for classification of SCC in sheep and goat related to quality of milk and infection status. These researchers suggested that infection of 25, 50 and 75 % of the udders in a given herd was associated with 4.1 to 12.2 % of milk loss in sheep and 0.8 to 2.3 % in goats . Mavrogenis et al.  suggested that an increase of 0.5 cells/mL × 106 SCC above the mean resulted in reduction of mean individual daily production of milk by 18 g.
In the present study, there was a 68 g difference in mean MY between infected and non- infected ewes. For SCC, the mean value for infected animals was approximately 3-fold higher than uninfected animals, similar to values reported in a previous study . However mean SCC for healthy animals were different. Mean SCC for uninfected animals was different to the value of 89 cells/mL × 103 reported by Pengov  and 311 cells/mL × 103 reported by Leitner et al. , and similar to the value of 1490 cells/mL × 103 reported by Kern et al. . These studies focused on Domestic Highland, East Friesand, and Awassi breeds, including their crosses and the Assaf breed, respectively. Moreover, considering the whole data set, mean SCC for infected animals was similar to reported values in the literature [4, 24]. Mean SCS for uninfected and mean SCS of whole data set were similar to the values reported in Valle del Belice [24, 25], and Churra dairy sheep breeds . For mean SCS of infected animals, Riggio et al.  reported a value of 6.42 and Leitner et al.  a value of 6.32 in Israel-Assaf and Awassi sheep, similar to the value of 6.21 obtained in our research. Another study reported lower values of mean SCS of infected animals using different breeds .
Our study confirms that CNS is the most prevalent etiological group of bacteria in the infected dairy ewes. The frequency of isolation of CNS on record (39 %) was lower than other studies ranging from 60 to 90 % [3, 24, 32, 34–36]. Moreover, a high percentage (77 %) of animals were found infected at least one or more times in the period of study, showing the importance of this group of bacteria in this population.
Most cases of CNS infection produce subclinical mastitis, although intramammary infections in its subclinical form by CNS have been described as the main single factor affecting udder health and profitability in small ruminants . Besides, due to the high prevalence of CNS during the ewe’s lactations, subclinical cases could persist, significantly increase SCC and consequently cause clinical mastitis. This is a possible explanation of the observed differences of SCC between infected and non-infected animals and frequency of animals infected by CNS. Moreover, considering the opportunistic nature of CNS , with adequate hygiene practices, correct milking routine and periodic revision of milking equipment, intramammary infections by CNS could be reduced.
In this investigation, CNS were classified as minor pathogens. Researchers have reported that some species of CNS can cause high SCC, similar to those of major pathogens [15, 32, 37] and even clinical mastitis [32, 38]. Ariznabarreta et al.  described that Staphylococcus caprae and S. simulans were associated with high log SCC, 6.43 and 6.35, respectively, in contrast with other CNS bacteria such as S. chromogenes, S. hominis, S. capitis, S. haemolyticus and S. epidermidis ranging from 5.93 to 6.09. Therefore, there was variation in the inflammatory response according to the involved CNS species and their pathogenicity in milk measured through SCC, even on average ten times higher than in dairy cattle . STHAU was the second one more frequently isolated bacteria in our study (5 %) followed by STR (3 %). This order differs from other authors, which reported that CNS is the most prevalent group of bacteria followed by STR [15, 31, 35, 38]. For STHAU, ewes infected at least one time or more in the period of study were 22 % (513). These findings are different respect to what reported by Riggio et al.  with values of 10.47 % of milk samples and similar to other studies ranging from 2 to 5.5 % [15, 32]. Infection due to STHAU is related with subclinical to acute clinical mastitis (gangrenous mastitis) with different clinical symptoms according to the virulence of the strains and in severe cases lead towards culling of the affected sheep [2, 17]. The high percentage of animals affected by STHAU in the period of study could be related with clinical mastitis cases and culling of ewes in this population. This was in agreement with Mavrogenis et al.  which identified STHAU as the most prevalent bacteria in clinical mastitis cases.
In sheep a heritability estimate of 0.09 for infection status assessed by bacteriological analyses was reported by Riggio et al.  and Tolone et al.  in the Valle del Belice breed using a threshold animal model assuming a probit link function. Gonzalo et al.  estimated genetic parameters of SCC in Churra sheep considering the type of mammary pathogen using a multitrait repeatability animal model. They reported that the effect related to the type of pathogen accounted for 32.5 % of the total variance in SCC, a value similar to that obtained for the residual effect (34.9 %), indicating a high relative importance of the type of pathogen in the decomposition of the variance for SCC. In addition, Holmberg et al.  in dairy cattle reported genetic variances for different pathogens ranging from 0.024 to 0.188, similar to the values of the present research (0.03 to 0.15). These results showed the importance of differentiating between the types of mammary bacteria assessed by bacteriological analyses in genetic mastitis studies.
Variances due to permanent environment and FYS effects were high and were important factors to explain the phenotypic variance resistance against CNS, STR and ALL. The possible explanations of these results for CNS group of pathogens are their nature and their high frequency of isolation in this sheep breed. CNS group of bacteria are related with inadequate management and hygiene practices, which could be different among the flocks, through the year and among them. Therefore, due to opportunistic nature of CNS, poor flock management and inadequate milking hygiene could increase the probability of occurrence of mastitis, and flocks may act as reservoirs of some CNS species. Taking into account the predominant sheep husbandry system in Sicily based on grazing with animals kept outdoors, reductions in pasture quantity and quality through the year as in summer (peak of lambing in Valle del Belice sheep) could be a stress factor to increase the susceptibility due to ALL infection. High temperatures in summer are associated with heat stress , and as occurs in dairy cattle heat stress is recognized as a factor which increases susceptibility to mastitis. Gonzalo et al.  reported that month within flock and flocks were accounted 44.1 % of the variance on bulk tank bacteria count, whereas Portolano et al.  reported that flock-year of lambing effect explains 27 % of the variance of time interval between lambing and first record with mastitis.
Heritabilities for pathogen-specific mastitis were in agreement with results of De Haas  in dairy cattle ranging from 0.02 to 0.10. However, this study only included heritabilities of pathogens involved in clinical mastitis cases and were estimated through threshold and linear models. For genetic correlations, the one estimated between CNS and ALL (0.92) was positive and very high suggesting that both are the same traits. This could be explained for the high frequency of isolation of CNS in the records (77 %). Thus, a high percentage of ALL group is explained by CNS pathogens. Furthermore, due to the fact that phenotypic variation for CNS and ALL is determined primarily by an environmental component both type of traits (CNS and ALL) could be controlled more effectively by applying a correct management measures instead of selective breeding on these population.
In the Valle del Belice breed, where the current selection is mainly practiced on a “within farm” approach and based on own performance of ewes, it is unlikely that selection for mastitis resistance is successful, independent of the use of infection status or SCS.
The results of our study support the presence of significant genetic variation for resistance to one specific pathogen causing mastitis (i.e. Streptococci). The high genetic correlation between ALL and CNS indicate that both are almost the same trait. The opportunistic nature of CNS and the high environmental influence of CNS resistance suggest that improvement of flock management and adequate milking hygiene could reduce significantly the incidence of mastitis caused by this pathogen in Valle del Belice dairy sheep.
A, animal; AF, absolute frequency; ALL, all pathogens together; BACIL, Bacillus spp.; CFU, five colony forming units; CNS, coagulase-negative staphylococci; CORLT, Corynebacterium spp.; ESCCL, Escherichia coli; FYS, flock year season; MY, milk yield; OP, order of parity; PASCL, Pasteurella spp.; PE, permanent environmental; PSELT, Pseudomonas spp.; RF, relative frequency; SCC, somatic cell count; SCS, somatic cell score; STHAU, Staphylococcus aureus; STPAG, Streptococcus agalactiae; STPDG, Streptococcus dysgalactiae; STPUB, Streptococcus uberis; STR, Streptococci; STR, Streptococcus spp
We acknowledge Dr. M.L Scatassa (Istituto Zooprofilattico Sperimentale della Sicilia) for bacteriological analyses.
No funding was obtained for this study.
Availability of data and materials
The data and pedigree supporting our findings are publicly available online at https://figshare.com/articles/data_txt/3467942 and https://figshare.com/articles/pedigree_txt/3467945, respectively.
MT and CL contributed equally to this work, they carried out the design of the study, performed statistical analysis and drafted the manuscript. JMY participated in statistical analysis and drafted the manuscript. SN helped to draft the manuscript and to interpret the results. MTS helped to collect the data and revised critically the manuscript. BP participated in the design of the study and gave the final approval of the version to be submitted. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
The milk samples were collected during routine milking so avoiding any harmful process to individuals. The milking procedure followed the A4 recording scheme which is defined by the International Committee for Animal Recording (ICAR, 2014). The consent for sample collection was obtained by the animals’ owners. Moreover, Sample collection, animal management and cares were in agreement with the Directive 2010/63/EU.
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