Seasonal variation of gastrointestinal parasitic infections in goats and sheep in São Luís, Maranhão, Brazil

ABSTRACT This study aimed to analyze the seasonal variation of gastrointestinal parasitic infections in goats and sheep in São Luís, Maranhão, Brazil. Fecal samples were collected directly from the rectal ampulla of the animals to count the eggs per gram in the feces at 30-day intervals over the 12-month study period. This study included 40 small ruminants, comprising 22 goats (14 sows, 6 kids, and 2 sires) and 18 sheep (13 sows, 4 lambs, and 1 sire). The study assessed the variation in the excretion of gastrointestinal nematode eggs during the dry and rainy seasons. Coproculture was performed to identify third-stage larvae. In the 12 months of research and monthly sample collections, 95.9% and 82.3% of the eggs detected were endoparasites in the fecal samples of the goats and sheep, respectively. Eimeria spp. oocysts were present in 50.6% and 30.4% of the goat and sheep fecal samples, respectively. The results indicated that the mean number of eggs per gram of feces was higher in the rainy season than in the dry season in both goats and sheep. The genera of gastrointestinal nematodes identified via monthly coproculture tests were Haemonchus sp., Trichostrongylus sp., and Oesophagostomum sp. Thus, gastrointestinal nematode parasitism was higher in goats and sheep during the rainy season than in the dry season, and the genera Haemonchus sp. and Trichostrongylus sp. were the most prevalent.


INTRODUCTION
Goat and sheep farming has become an important agricultural activity in Brazil.Brazil's Northeast region has great farming potential due to its large herds and suitable soil and climatic conditions (Silva et al., 2019) The occurrence of diseases and death in herds is directly associated with poor sanitary management, which limits the development of goat farming in the Northeast region (Fonseca et al., 2013).GI parasitic infection, one of the main sanitary issues for goat and sheep farmers, causes significant economic losses and high mortality rates (Suarez et al., 2017;Brito et al., 2018;Jansen et al., 2020).Charlier et al. ( 2020) stated that the host, climate changes, anthelmintic resistance, and environmental factors could change the epidemiology of GI parasites, thus increasing the need for adequate and sustainable control strategies.Understanding these interactions is crucial for designing adequate control measures.Biologic information of parasites helps to estimate the distribution and formulate integrated parasite management programs (Zajac & Garza, 2020).The environmental conditions and pasture microclimate of the pasture production system influence the development and survival of free-living GI nematodes, which could favor the migration of third-stage larvae (L3) inhabiting the soil, base of the clumps, and/or structure of the grazed forage plant (Roberto et al., 2018).Seasonal variation is an important decision-making parameter in the herd's parasitological evaluation, because climatic conditions after winter become favorable for the development and survival of eggs and larvae in the soil and pasture contamination, thus increasing the risk of infection in animals in the summer and fall (Tariq et al., 2010).This study aimed to assess the seasonal variation of GI parasitic infections in goats and sheep in São Luís, MA, Brazil.

MATERIAL AND METHODS
This study was conducted at the Federal Institute of Maranhão (IFMA), São Luís-Maracanã campus, São Luís, MA, Brazil, with geographic coordinates 2º36' 48" S and 44º16' 41" W. Animals from the sheep and goat farming sector were used.These goats and sheep grazed together in an area comprising three pasture paddocks of 0.8 hectares equipped with drinkers and covered troughs.The research project was approved by the IFMA Animal Research Ethics Committee (Approval No. 02/2021).The research was conducted over 12 months from October 2021 to September 2022, and it included 22 goats (14 sows, 2 sires, and 6 kids) and 18 sheep (13 sows, 1 sire, and 4 lambs).The animals were subjected to semi-intensive management with the roughage part of their diet consisting of Megathyrsus maximus cv.Massai grass.They spent 8 hours grazing daily and received concentrate feed equivalent to 3% of the live weight at the end of the day (Table 1).

RESULTS & DISCUSSION
The EPG counts were used to determine the average monthly infection in the studied herds (mean EPG) and its relationship with the local meteorological conditions (NuGeo/UEMA) (Table 2).Figure 1 shows parasitic infection variation with environmental changes, highlighting the increased mean EPG count in the months with the highest rainfall indices in the rainy season.v.36, n.1, p.73-87, 2020.
http://dx.doi.org/10.1590/S1519-994020230020ISSN 1519 9940 2 were identified as described byUeno &  Gonçalves (1998).Thus, data were collected monthly over 12 months to measure the variation in the GI nematodes in the dry and rainy seasons.Meteorological indices (rainfall, temperature, and relative humidity) were recorded for each monthly sample survey from the Geoprocessing Center (NuGeo) of the State University of MA (UEMA).In São Luís, the rainy season occurs from January to June, and the dry season from July to December.Microsoft Office Excel version 2010 was used for data processing.The descriptive method and tabular analysis technique were used to analyze and interpret data.Data of the selected variables are presented as absolute and relative frequencies and as means ± standard deviations.

Figure 1 .
Figure 1.Mean eggs per gram counts in goats and sheep and rainfall index (mm) between October 2021 and September 2022 in São Luís, Maranhão, Brazil (EPG, eggs per gram) . The Brazilian herds include approximately 12.1 million goats and 20.6 million sheep; the Northeast region has the largest herds, accounting for approximately 95% and 70% of the country's goats and sheep, respectively.

Table 1 .
Diet composition (Gordon & Whitlock, 1939)ted directly from the rectal ampulla of the animals to count the eggs per gram (EPG) in the feces at 30-day intervals as described previously(Gordon & Whitlock, 1939).The tests were conducted at the IFMA Laboratory of Animal Health, São Luís-Maracanã campus.Larval culture was performed according to the Roberts & O'Sullivan technique(1950), and L3

Table 2 .
Suarez et al. (2013)ounts and meteorological indices from each monthly sampling survey in goat and sheep herds in São Luís, Maranhão, Brazil from The results of this study showed that the mean EPG count in both the evaluated animal species was 2,498 in the rainy season and 1,817 in the dry season.The mean EPG count increased in both species in the rainy season.During the rainy season, environmental factors such as rainfall and temperatures favor the free-living stages of GI nematodes(Dias et al., 2022).Similar results were reported bySuarez et al. (2013)in tracer kids, with a four-fold higher number of GI nematodes in the rainy period than in Jansen et al. (2020) SD, standard deviation) GI nematodes accounted for 95.9% and 82.3% of the eggs detected in the fecal samples of goats and sheep, respectively, during the 12-month study period.The frequency of Eimeria spp.oocysts was 50.6% in goats and 30.4% in sheep.Brito et al. (2009)examined 192 goat fecal samples in the south-central region of MA and reported that 176 (91.66%) were positive for GI nematode eggs, while 134 (69.79%) contained oocysts of the genus Eimeria.Moreover, of the 192 sheep fecal samples examined, 122 (63.54%) were positive for GI nematode eggs, while 113 (58.85%) contained oocysts of the genus Eimeria.Additionally, Moniezia sp.eggs were present in 19 (9.90%) goat samples and 8 (4.17%) sheep samples.Kelemework et al. (2016) studied helminth infection in 384 fecal samples from goats and sheep in Ethiopia and reported an infection rate of 91.4% in sheep and 86.2% in goats.Dey et al. (2020) studied GI nematodes in 1,998 goats from Bangladesh, of which 1,241 (62.1%) were infected with one or more species of GI nematodes.The identified nematodes included strongyles (51.9%),Strongyloides sp.(19.0%), and Trichuris spp.(2.9%).Similar results were reported by Salas et al. (2016), who studied the prevalence of GI nematodes in goats and sheep in Colombia and reported that 76% of the animals were infected.thedryperiod.This study corroborates the findings ofGana et al. (2015), who studied goats and sheep in Nigeria and reported a high prevalence of GI nematode infections in the rainy season.However,Dey et al. (2020)found no statistical difference between the EPG counts of goats in the rainy and dry periods in seven regions of Bangladesh.Atanásio-Nhacumbe et al. (2019) analyzed the prevalence and seasonal variation of GI nematodes in goats in Mozambique and reported the highest prevalence and EPG counts in the rainy season, demonstrating an obvious seasonal pattern.Jansen et al. (2020)studied the prevalence and seasonal variation of GI nematodes and coccidia in sheep in South Africa.They reported a significantly high prevalence of GI nematodes in the humid zone (H.contortus, 81%; Eimeria sp., 37%), followed by the semi-humid zone (H.contortus, 75%; Eimeria sp., 22%), and the lowest prevalence in the arid zone (H.contortus, 71%; Eimeria sp., 14%).

Clinics of North America: Food Animal Practice,
Dias et al. (2022)))reported a range of 400-2,327 in dairy goats in Argentina.Both studies presented values lower than those reported in this study.In Nigeria,Gana et al. (2015)reported that the mean EPG count of the family Strongyloidea was 4,208 in sheep and 2,630 in goats.These counts differed from the results of this study, which showed a higher parasite load in goats than in sheep, considering the variations in the study period.Coproculture revealed mixed infections, with Haemonchus sp.being the most prevalent parasite genus, presenting more than 95% of infective larvae in goats and sheep in some months (Figures2 and 3), followed by Trichostrongylus sp. and Oesophagostomum sp.Sousa et al. (2018)found H. contortus as the main larva (73.5%), followed by T. colubriformis and O. columbianum.Similar results were shown byDias et al. (2022)when studying the prevalence of GI helminths in goats in the Baixo Parnaíba region, Piauí, Brazil.They reported a prevalence of 84% of Haemonchus sp., 13% of Trichostrongylus sp., and 0.3% of Oesophagostomum sp.Mushonga et al. (2018) studied the prevalence of H. contortus in goats and sheep in Rwanda and reported an overall infection prevalence of 75.7% in both.The prevalence of H. contortus infection was higher in sheep than in goats (83.4% vs. 71.8%).Percentage of infective third-stage larvae of gastrointestinal nematodes in the coproculture of sheep samples from October 2021 to September 2022 in São Luís, Maranhão, Brazil A study of the effects of GI nematodes in dairy goats in Argentina by Suarez et al. (2017) corroborates the findings of this study regarding the prevalent genera, since they identified Haemonchus sp.MA, Brazil.Moreover, the degree of parasitism was higher in goats than in sheep.The genera of GI nematodes identified in the monthly coproculture revealed the presence of Haemonchus sp., Trichostrongylus sp., and Oesophagostomum sp. in the goats and sheep.Technological Development for the grant and the Federal Institute of Maranhão for the financial resources and infrastructure.TARIQ, K.A.; CHISHTI, M.Z.; AHMAD, F. Gastro-intestinal nematode infections in goats relative to season, host sex and age from the Kashmir valley, India.Journal of Helmintology, v.84, n.1, p.93-97, 2010., X.; LIU, M.; HE, S.; TONG, T.; LIU, Y.; DING, K.; WANG, P.An epidemiological study of gastrointestinal nematode and Eimeria coccidia infections in different populations of Kazakh sheep.PLoS ONE, v.16, n.5, e0251307.https://doi.org/10.1371/journal.pone.0251307,2021.ZAJAC, A.M. & GARZA, J. Biology, Epidemiology and Control of Small Ruminant Gastrointestinal Nematodes.Veterinary and Trichostrongylus sp. as the most prevalent genera during their 11-month research.In addition to these two genera, they identified a small percentage of the genus Teladorsagia.Yan et al. (2021) conducted an epidemiological study on sheep in Kazakhstan and identified H. contortus, Trichostrongylus spp., and Ostertagia spp. as the predominant species.The epidemiological study of GI nematodes in small ruminants in Nigeria by Gana et al. (2015) identified two genera of adult abomasal nematodes, Haemonchus sp. and Trichostrongylus sp.The prevalence of Haemonchus sp. and Trichostrongylus sp. were 78.5% and 17.5% in goats and 85% and 31% in sheep, respectively.Kelemework et al. (2016) identified the following six genera of nematodes in the coproculture of both goat and sheep samples in ACKNOWLEDGMENTS The authors would like to thank the National Council for Scientific and YAN