Elsevier

Veterinary Parasitology

Volume 287, November 2020, 109274
Veterinary Parasitology

Interaction between abomasal blood feeder Haemonchus contortus and intestinal mucosal browser Trichostrongylus colubriformis during co-infection in Boer goats

https://doi.org/10.1016/j.vetpar.2020.109274Get rights and content

Highlights

  • H. contortus and T. colubriformis interacted with each other in Boer goats.

  • T. colubriformis contributes more to the variation of FEC than H. contortus.

  • Co-infection induced an IgA response but only protective against T. colubriformis.

  • IgA effects differ for H. contortus and T. colubriformis infections in goats.

  • T. colubriformis length related to low number and composite burden of H. contortus.

Abstract

This study was conducted to investigate potential interactions between the abomasal blood feeder Haemonchus contortus and the intestinal mucosal browser Trichostrongylus colubriformis among deliberately infected Boer goats. Faecal and blood samples were collected twice a week for eight weeks from 25 parasite-naïve goats. Correlation analysis and multiple linear regression models were conducted to explore the association between phenotypic variables and variables taken at necropsy. Positive associations were identified between total FEC and log T. colubriformis number (r = 0.62, p < 0.05) as well as between IgA and peripheral eosinophil counts (r = 0.65, p < 0.05). A negative correlation was observed between T. colubriformis and log H. contortus number (r=-0.56, p < 0.05). Multiple linear regression models show that H. contortus and T. colubriformis interacted with each other. T. colubriformis appeared to contribute more significantly to the variation of FEC than H. contortus. Co-infection induced an IgA response which was only effective against T. colubriformis but not protective against H. contortus infection. This could be seen via significant associations of IgA with both nematode species but with the effect of IgA differing for H. contortus and T. colubriformis. In this study, H. contortus infection was not detrimental to the goats with no observed impact on PCV. This could be because the growth of T. colubriformis as represented by its length was associated with reduced number and composite burden of H. contortus during co-infection, or possibly due to low infection dosage. Improved understanding of the impact of H. contortus and T. colubriformis and their interaction from natural co-infection studies is beneficial for a better understanding of the goat-parasite interaction and its potential impacts on the health and productivity of animals.

Introduction

Infection by mixed gastrointestinal nematodes is common in natural infections among small ruminants and could affect their productivity. In tropical and subtropical countries, Haemonchus contortus is known as the most pathogenic nematode of small ruminants particularly due to its high biotic potential and blood sucking ability (Waller and Chandrawathani, 2005), and thus it has been a focus of scientific research. Anaemia, lack of appetite, lethargy, loss of weight, dehydration, oedema and subsequent death in heavy infections are the common signs of haemonchosis (Getachew et al., 2007; Besier et al., 2016; Emery et al., 2016). In contrast, little attention has been paid to Trichostrongylus colubriformis infection which shows milder signs than those of haemonchosis (Cardia et al., 2011).

Milk production in Saanen goats that have been treated for natural infection with H. contortus and T. colubriformis is higher (399.5 L ± 34.0 L) than the untreated groups (281.6 L ± 37.5 L) (Suarez et al., 2017). In repeated deliberate infection with H. contortus and T. colubriformis on naïve dairy goats, the high milk producers suffer from severe pathophysiological disturbances that lead to low milk yield (Chartier and Hoste, 1997). However, most of the research on natural infection has been conducted in sheep (Doligalska et al., 1999; Bishop and Stear, 2000; Mugambi et al., 2005) rather than goats.

The interaction between H. contortus and T. colubriformis in deliberately infected sheep has been explored and it has been shown that co-infection affects both nematode species as well as cellular immune response of the host (Lello et al., 2018). In this study, the immune response induced by T. colubriformis had negative impacts on the number of H. contortus. In contrast, immune suppression caused by H. contortus had a positive impact on the number of T. colubriformis. To our knowledge, no similar study has been conducted to investigate the potential interactions in goats.

Assessing potential interactions between nematode species requires information on several characteristics including nematode number, nematode length and composite worm burden. Nematode length is a marker of its fecundity but both characteristics (length and fecundity) are influenced by the number of nematodes within the host as well as by the strength and specificity of IgA response (Stear et al., 1999a,b). Reduction in the length and fecundity of adult nematodes is one of the signs of immunity in sheep which is strongly associated with the local IgA and eosinophil response (Stear et al., 1995; Henderson and Stear, 2006). In addition, faecal egg counts (FEC) and packed cell volume (PCV) as indicators of worm burden (Saddiqi et al., 2012; McRae et al., 2015) can be considered to investigate the interaction between nematode species and its effects on the host.

The aim of this study was to investigate potential interactions between H. contortus and T. colubriformis in goats by exploring the association of H. contortus and T. colubriformis composite burden, length and numbers, and the effect of IgA and peripheral eosinophil counts on these variables during co-infection; and to identify significant explanatory variables for FEC and PCV during co-infection of H. contortus and T. colubriformis.

Section snippets

Field and laboratory work

Faecal and blood samples were collected twice a week for eight weeks at three-four-three day intervals from 25 naïve Boer goats that were deliberately infected with H. contortus, T. colubriformis and Oesophagustomum spp. Four goats served as negative control. The faecal samples were subjected to the modified McMaster technique and the blood samples were used to measure IgA, PCV and peripheral eosinophil counts. The details of study sites and animals, animal ethics, and the field and laboratory

Phenotypic data and nematode variables

The mean of phenotypic data such as FEC, IgA, PCV and eosinophil counts throughout 16 times of sampling are shown in Table 1. The mean length of male and female H. contortus and T. colubriformis that have been collected from the abomasum and small intestine of each goat as well as the composite worm burden are also shown. The species, sex and number of nematodes collected from each goat in the abomasum and small intestine have been reported previously in Basripuzi et al. (2020).

Correlation analysis between variables

Table 2 shows

Discussion

This study explored the effects of a single, low-dose deliberate infection of mixed gastrointestinal L3 in naïve Boer goats. This infection was predominately H. contortus followed by T. colubriformis with the L3 of Oesophagostomum spp. failing to develop to adult stage (Basripuzi et al., 2020). Therefore, this study focused on analysing the interaction between gastrointestinal nematodes that were recovered during total worm count procedure, namely H. contortus and T. colubriformis.

This study

CRediT authorship contribution statement

N. Hayyan Basripuzi: Conceptualization, Methodology, Investigation, Formal analysis, Writing - original draft, Writing - review & editing, Visualization. Reuben S.K. Sharma: Supervision, Resources. Z. Norhadila: Investigation. Z.S. Shahar: Investigation. M.S. Nor-Dilaila: Investigation. M.S. Mustapha: Investigation. V. Kolandaiveloo: Investigation. K. Ruviniyia: Investigation. L. Matthews: Supervision, Conceptualization, Methodology, Software, Formal analysis, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We would like to acknowledge Parasitology Laboratory, Faculty of Veterinary Medicine, Universiti Putra Malaysia where the laboratory works have been conducted.

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