The results of this study reveal a serious situation of GIN parasitism in sheep farms in the department of Córdoba. All of the farms sampled showed cases of gastrointestinal parasitism, where 88.6% of the animals were affected with one or more types of nematodes. Although parasitic infection was expected due to an apparent predisposition of the sheep, it is important to note that the seriousness of this finding lies not only in the prevalence of parasitism but also in the high parasite burdens, which averaged 1255 EPG/animal; this value is considered a high-level infection, taking into account the classification of infection levels according to Hansen and Perry (1994). Considering the parasitic groups, high-level infections were found to be caused by Strongylida nematodes, mostly from the Trichostrongylidae family, which harbors genera of importance in sheep due to their high pathogenicity such as Haemonchus contortus (Wang et al. 2020) and whose parasitic burdens in this study showed a significant association with clinical factors such as body condition, hematocrit and FAMACHA score. Strongyloides spp. infections were considered moderate and Trichuris spp. infections low.
Dewormed animals and those with recent deworming before McMaster tests, presented the highest Strongylida and Strongyloides spp. burdens; this contradictory situation may be explained as a desperate need of producers to apply anthelmintics due to the inefficient reduction of parasite burdens; in the study, we observed that different farms performed monthly application of anthelmintics; these results suggest signs of anthelmintic resistance, especially related to the infections due to Strongylida nematodes.
Regardless of the type of anthelmintic used, parasite burdens were high, suggesting a possible inefficiency of fenbendazole, ivermectin, levamisole and the use of natural medicine in the control of parasitism. It should be noted that in the overall count and the Strongylida order, lower burdens were found in sheep that had been treated with levamisole. The development of anthelmintic resistance, especially to ivermectin and fenbendazole, has been previously reported in several studies (Torres-Acosta et al. 2012). This result reflects the need to implement monitoring programs to assess the efficacy of anthelmintics used in the parasitic control of sheep.
The degree of infection by Trichuris spp. did not differ according to the type of anthelmintic used; it is necessary to point out that burdens of this parasitic group were very low, which cannot suggest the effectiveness of the anthelmintics used since there was also no difference between dewormed and non-dewormed animals and between the time of the last deworming; this result is rather associated with the low prevalence and low burdens of Trichuris spp. in the department of Córdoba.
The GIN infection prevalence and parasite burdens were similar in males and females. Most studies address the influence of sex on GIP prevalence and in general, there is no consensus on which sex is more affected (Poddar et al. 2017).
Productive stage was not associated with overall parasite burdens or Strongylida infections. However, there is a trend of higher burdens in rearing animals and lactating ewes. In that sense, several studies agree that young animals are more susceptible to gastrointestinal parasitism (Raza et al. 2007) since they have an immune system with insufficient development to modulate parasitic infestation (Khan et al. 2010); on the other hand, it is known that regardless of the year, season and age, ewes present greater susceptibility to GIN during lactation (González-Garduño et al. 2014). Experimentally, there are studies that support the hypothesis that full grown animals can acquire immunity against GIN (Knox 2000). Regarding the degree of infection, Ensuncho et al. (2014) reported that lactating animals and lactating ewes presented the highest parasite burdens.
Breed was associated with overall GIN parasite burden and particularly for Strongylida and Strongyloides spp. nematodes. It was observed that breeds belonging to OPC had lower parasite burdens. Breeding studies of small ruminants have revealed a reduction of EPG in faeces when animals that are naturally resistant to GIN infection are selected for breeding (Eady et al. 1996). Genetic factors are known to contribute to the ability of sheep to cope with the challenge of intestinal parasitism; some studies have shown that different breeds of sheep exhibit varying resistance to intestinal parasite infection (Aboshady et al. 2020). In particular, Preston and Allonby (1979) demonstrated an ascending order of susceptibility in the Red Masai, Blackhead Persian, Merino, Dorper, Corriedale and Hampshire breeds. However, other undesirable traits, especially in terms of productivity, could make parasitism-resistant breeds unattractive to producers (Woolaston and Baker 1996). In this regard more recent studies, have shown that genome-wide selection strategies can improve selection of animals with a view on production aspects and helminthiasis resistance traits (McManus et al. 2014).
The clinical variables analyzed, namely: body condition, hematocrit and FAMACHA® result, were especially related to high parasite burdens by Strongylida. Animals with the highest degrees of infection showed fair or poor body condition, low hematocrit values and higher FAMACHA® results. For Strongylida nematodes, the FAMACHA® method had a better predictive value, followed by hematocrit and body condition; Strongyloides spp. infections were correlated only with hematocrit and body condition. The above allows to state that the alteration of the clinical variables and their use as predictive value of the parasitic burden, will depend on the parasitic group that is affecting the animals.
The most prevalent nematode genera are associated with the percentage of larvae identified from the faecal cultures. Trichostrongylus spp., Strongyloides spp. and Haemonchus spp. were the most prevalent genera in sheep in the department of Córdoba. These have been previously reported (Ensuncho et al. 2014). It is important to highlight, that it was found for the first time for the department of Córdoba, Bunostomum spp. nematodes comprising GIN infections in sheep. Although they were only identified in 10% of the flocks studied, their hematophagous behavior, as well as that of H. contortus, causes a decrease in hematological values, including hemoglobin, with immediate consequences such as hypoproteinemia and a decrease in body condition. Analyzing these clinical aspects is important when making decisions regarding deworming management in sheep production systems; Besier et al. (2016) indicate that a good body condition may indicate the ability of sheep to better cope with parasitism. Increasing resistance to anthelmintics has resulted in developing deworming management alternatives, which reduce the selection resistant parasites, being essential. In this regard, a suitable approach would be to treat only those animals that are unable to cope with the parasite challenge.
The clinical evaluation of anemia using the FAMACHA® system and the body condition of the animals are two important clinical aspects to examine a flock and identify animals that do require anthelmintic treatment (Van Wyk and Bath 2002), these selective deworming programs could be considered within the strategies implemented in the flocks to delay the development of resistance. In the present study, it is evident that the FAMACHA® Method and the measurement of body condition can be used to establish selective deworming programs in herds in the department of Córdoba, since a significant association with parasite burden was found.
Gastrointestinal parasitism in sheep is a worldwide issue, which requires a deeper understanding of epidemiological aspects such as prevalence, distribution and seasonal patterns of transmission in different climatic zones. There is a strong belief that climate change may alter the geographical distribution of parasites and their impact on hosts, a situation that is also attributed to the phenomenon of resistance (Chalier et al. 2014). It is believed, that climatic changes would have profound effects on the epidemiology of parasites, especially for those, whose developments outside the definitive host are sensitive to temperature and humidity linked to rainfall. The influence of environmental conditions is particularly evident in spatial distribution studies that allow the visualization of clusters where animals show not only the prevalence of gastrointestinal parasitism, but also high levels of infection, a parameter that is very interesting to predict the damage caused to individuals and the economic losses of the producer.
The results of this study reveal a serious situation of gastrointestinal parasitism in sheep production systems in the department of Córdoba. All the farms studied are infected by gastrointestinal nematodes; however, the identification of two high density clusters allows directing epidemiological and control studies to these areas. The results suggest a possible resistance to anthelmintics used by the producers, a situation that requires further evaluation.