Gastrointestinal trichostrongylosis can predispose ewes to clinical mastitis after experimental mammary infection

doi:10.1016/j.vetpar.2017.08.013

Veterinary Parasitology

Volume 245, 15 October 2017, Pages 71-77

https://doi.org/10.1016/j.vetpar.2017.08.013 Get rights and content

Highlights

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Sheep: role of gastrointestinal nematode infection in predisposing to mastitis was studied.
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Gastrointestinal trichostrongylosis might lead to clinical mastitis.
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Effect of Teledorsagia helminths was more significant.
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Various pathogenetic pathways can be involved.

Abstract

Objective was to study, in an experimental model, the possible role of gastrointestinal nematode infection in predisposing ewes to mastitis during the lactation period. Twenty-four ewes (A or B [n = 12]), free from nematode and trematode helminths, were used. Group A animals received 5000 third-stage larvae of a trichostrongylid helminth cocktail and group B ewes were unparasitised controls. Animals in group A developed gastrointestinal trichostrongylosis confirmed by >500 epg in faecal samples; mean epg of group B ewes were <20 (P < 0.001). Ewes were challenged by deposition of Mannheimia haemolytica into the teat duct. In group A, 7 ewes developed clinical and 5 subclinical mastitis; no ewe in group B developed clinical mastitis, but only subclinical (12 ewes) (P = 0.002). M. haemolytica was isolated from 132/132 and 121/132 udder samples from group A or B, respectively (P < 0.015); increased leucocyte numbers were recorded in 66/66 and 61/66 samples, respectively (P = 0.023). During post-mortem examination, mean number of helminths in gastrointestinal content was 2523 and 7.5 in group A or B, respectively (P < 0.001); within group A, proportions of Teladorsagia and Haemonchus were significantly greater in ewes that developed clinical mastitis than in others which did not (0.709 and 0.162 versus 0.662 and 0.136, respectively; P < 0.035). M. haemolytica was isolated from 36/36 and 19/36 udder tissue samples from group A or B, respectively (P < 0.001). In ewes with subclinical mastitis (in group A or B), inducible-lymphoid-follicles were observed in the teat, which were not observed in ewes with clinical disease. Total pathology scores summed over all days were 127 and 73 for group A or B ewes, respectively (maximum possible 192; P < 0.05). In general, there was positive correlation between intestinal helminth counts and pathology score (P < 0.001) and between Teladorsagia counts and pathology score (P = 0.002) in ewes that developed clinical mastitis. It is concluded that, in view of bacterial challenge, gastrointestinal trichostrongylosis and particularly Teladorsagia infection, might lead to clinical mastitis, through various pathogenetic pathways.

Introduction

Mastitis and gastrointestinal trichostrongylosis are two significant health problems of sheep. Control programs are available for both conditions, but, nevertheless, the disorders are still widely prevalent in sheep flocks around the world. Mastitis control programs give emphasis in reducing the rate of mammary infections during milking routine, when mammary glands are at the greatest risk for infection. However, various other factors outside the milking routine (environmental, nutritional, genetic, anatomic, nosological) have been identified to predispose ewes to mastitis (Bergonier and Berthelot, 2003, Gelasakis et al., 2015, Fthenakis et al., 2017). Objective of the present work was to study, in an experimental model, the possible role of gastrointestinal nematode infection in sheep, which is the most prevalent infection in those animals worldwide, in predisposing ewes to mastitis during the lactation period.

Section snippets

Study design

In total, 24 secundigravidae (i.e., in second pregnancy) ewes (Karagouniko-cross breed) were included into the study. When animals were introduced into the study, they were pregnant, bearing one lamb (confirmed by repeated ultrasonographic examinations), after a standard reproductive protocol (intravaginal use of progestagen sponges) had been applied to synchronise their oestrus cycles. Ewes were selected for inclusion into the study among animals with no history of clinical mastitis during

Clinical findings

All ewes lambed normally one lamb, within a period of 7 days. No clinical abnormalities had been recorded in any animal before mammary challenge (after lambing and on D-1). In group A, in the inoculated side of the udder, 7 ewes developed clinical (incidence: 0.586) and 5 ewes subclinical (incidence: 0.414) mastitis. In group B, in the inoculated side of the udder, all 12 ewes developed subclinical mastitis (incidence: 1.000). There was clear evidence (P = 0.002) of a significant difference in

Discussion

Gastrointestinal trichostrongylosis, which has a worldwide dissemination, is the most frequent infection of sheep (Kaplan and Vidyashankar, 2012, Taylor, 2012). Most often, the infection does not lead to disease, but, nevertheless, adversely affects production of animals (Mavrot et al., 2015).

Clinical mastitis, apart from the obvious financial significance, especially in dairy production flocks (Gelasakis et al., 2015), has also been considered as the most significant welfare problem in ewes

Conflict of interest statement

The authors have nothing to disclose.

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Interactions between parasitism and milk production - Mastitis in sheep
2019, Small Ruminant Research
Citation Excerpt :
In two recent publications, Mavrogianni et al. (2017) and Kordalis et al. (2019) have shown the effects of gastrointestinal nematode infections to development of mastitis in ewes. Mavrogianni et al. (2017) have used an experimental approach, by infecting ewes with a cocktail of larvae of trichostrongylid helminths and then challenging them with Mannheimia haemolytica into their teat duct. They found that parasitised ewes developed clinical mastitis after bacterial challenge and that the parasitised ewes lacked the inducible-lymphoid-follicles in the teat, which have been found to have a confirmed protective role for the mammary gland (Mavrogianni et al., 2005, 2006).
The present review discusses interactions and focuses in the direct effects of parasites in production of milk and development of mastitis in ewes. In most relevant published studies, a clear reduction in milk yield of ewes affected with parasites has been recorded. This reduction in milk yield has been quantified to average 22% among the relevant studies. Nematode parasitism can also cause shorter persistency of lactation, whilst the situation regarding potential effects on milk composition is not clear. Moreover, in field and experimental studies trichostrongylid intestinal infections have been documented to increase risk of mastitis in affected ewes; among parasitic species, the effect was associated primarily with Teladorsagia spp. infection. Trematode infection has also been found to increase risk for mastitis development at the early stage of lactation period. Research supports that effective parasite control will enable sheep to fully express their genetic potential and benefit for increased milk yield and effective udder health management schemes.
Evaluation of the pour-on administration of eprinomectin on milk yield and somatic cell counts in dairy ewes naturally infected with gastrointestinal nematodes
2019, Veterinary Parasitology: X
Citation Excerpt :
It is well known that GIN parasitism and especially Teladorsagia spp. can lead to protein and therefore, immunoglobulin deficiency (Stear et al., 2003). GIN parasitism suppresses the defense mechanisms of the mammary gland of the ewe predisposing to increase of SCC and appearance of clinical (Mavrogianni et al., 2017) or subclinical mastitis (Kordalis et al., 2019). According to Coop and Kyriazakis (1999), reduced energy availability has been recorded during trichostrongylosis (i.e. parasites engage energy sources) which can lead to decreased neutrophil function (i.e. delayed mobilization to the mammary gland, impaired phagocytosis, inefficient intracellular killing) contributing to mastitis (Mavrogianni et al., 2017).
The effect of pour-on eprinomectin administration on milk yield and somatic cell counts was studied in dairy ewes located on twelve farms in mainland Greece. On each farm, the selected ewes were randomly divided into three similar groups. Group 1 consisted of 10–15 untreated ewes (control group), Group 2 consisted of 10–13 ewes treated with a single dose of eprinomectin at Day 0 and Group 3 consisted of 6 ewes repeatedly treated with eprinomectin at Days 0, 42 and 70. Faecal egg counts and coprocultures were performed on Days 0, 7, 14, 28, 42, 56, 70, 84 and 98. The milk yield and somatic cell counts were measured. The topically administered eprinomectin was highly effective against gastrointestinal nematodes up to 42 days post treatment (94.1% and 99.7% for Groups 2 and 3, respectively). This beneficial effect was extended from Day 42 to 98, in ewes of Group 3. Ewes treated once or thrice presented an increase of daily milk yield by ca. 5% (50 mL/day) and 11% (105 mL/day), respectively, compared to untreated ewes. At the same frame, a significant decrease in somatic cell counts was observed in the eprinomectin treated ewes compared to the untreated ones. In conclusion, this study confirmed the high antiparasitic efficacy and the beneficial effect of pour-on eprinomectin on the milk yield and somatic cell counts in dairy ewes under semi-intensive management.
Field evidence for association between increased gastrointestinal nematode burden and subclinical mastitis in dairy sheep
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Indeed, mammary defence relies primarily on leucocytes, which provide a non-specific defence mechanism against invading pathogens (Fragkou et al., 2017). In the experimental study by Mavrogianni et al. (2017), we have provided evidence and we have discussed various pathways through which udder defences would be impeded by heavy parasitic infections, thus leading to development of clinical mastitis: the evidence in that study indicated that cellular defences in the udder of infected ewes had been depleted, thus increasing risk for development of clinical mastitis. During the study, the association of gastrointestinal nematode parasitism with presence of subclinical mastitis has only been identified at animal level and not at farm level.
The objective of the present study was to study, under field conditions, potential associations between gastrointestinal nematode parasitism and subclinical mastitis in ewes during the lactation period. Faecal and milk samples were collected from 240 ewes in 16 farms, for parasitological and bacteriological plus cytological examination, respectively. In the population sampled, prevalence of gastrointestinal nematode infection was 63.0%; mean faecal count was 357.7 ± 32.4 eggs per gram (epg); Teladorsagia spp. larvae were identified more frequently in coprocultures (median proportion among farms: 53.0%). The prevalence of subclinical mastitis was 22.6%; coagulase-negative Staphylococcus spp. were identified more frequently as causal agents (64.7% of isolates recovered from cases of the disease). There was clear evidence that the prevalence of subclinical mastitis was higher among ewes with gastrointestinal nematode infection than among ewes without: 26.4% and 16.1% (P = 0.047), respectively. Further, the prevalence of subclinical mastitis was higher in ewes with high faecal epg: 31.1% versus 18.6% in ewes with low faecal epg (P = 0.027). Mean epg counts in ewes with mastitis were significantly higher: 500 ± 84 (mean ± standard error of the mean), than epg counts in healthy ewes: 316 ± 36 (P = 0.024). The findings further underline the importance of concurrent parasitic and bacterial infections. Moreover, results also suggest further factors that can play a role in development of mastitis in ewes.
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Research paperGastrointestinal trichostrongylosis can predispose ewes to clinical mastitis after experimental mammary infection

Highlights

Abstract

Introduction

Section snippets

Study design

Clinical findings

Discussion

Conflict of interest statement

Parasitol. Int.

Small Rumin. Res.

Small Rumin. Res.

Livest. Prod. Sci.

J. Trace Elem. Med. Biol.

Vet. Parasitol.

Vet. J.

J. Comp. Pathol.

Vet. J.

Br. Vet. J.

Anim. Reprod. Sci.

Small Rumin. Res.

Small Rumin. Res.

Vet. Microbiol.

Trans. R. Soc. Trop. Med. Hyg.

Vet. Immunol. Immunopathol.

Vet. Parasitol.

Small Rumin. Res.

Vet. Parasitol.

Small Rumin. Res.

Small Rumin. Res.

Vet. Clin. N. Am. Food Anim. Pract.

Small Rumin. Res.

Small Rumin. Res.

Vet. Parasitol.

Manual for the Identification of Medical Bacteria

Cytokine concentrations in the blood of ewes that had developed pregnancy toxaemia, as well as in the blood of their lambs

Research paper
Gastrointestinal trichostrongylosis can predispose ewes to clinical mastitis after experimental mammary infection