INTRODUCTION

Gastrointestinal nematode infections affect the health of small ruminants compromising their production and reproduction, more frequently in young developing animals, causing low weight gain and growth retardation, making them one of the main causes of economic losses (^{González et al., 2011}; ^{Asmare et al., 2016}; ^{Kuma et al., 2019}), mainly in the costs incurred in treatment and control (^{Tramboo et al., 2015}). Sheep are generally more prone to gastrointestinal parasitism, due to their feeding on larvae 3 contaminated pastures (^{Tariq et al., 2008}). Among gastrointestinal parasites, Haemonchus is the species with the highest economic importance (^{Rinaldi et al., 2015}). This nematode is located in the abomasum, feeds on the blood of sheep and goats, can be found in other ruminants such as cattle (^{Getachew et al., 2007}), it is among the most pathogenic in sheep (^{Besier et al., 2016}), its extensive geographical distribution and resistance against anthelmintic control measures makes it a threat to the sustainability of sheep farming (^{Saccareau et al., 2017}). The rainy season favors its frequency, with animals grazing during the early morning hours (^{Mederos et al., 2010}), the prevailing climate (temperature, rain and humidity) and management practices in husbandry are considered the main factors driving its distribution (^{Rinaldi et al., 2015}); its distribution is heterogeneous and depends on variables that differ from one area to another, even from one farm to another, such as management, prevention and control (^{Musella et al., 2011}). On the other hand, studies on the prevalence in grazing animals is high in areas with tropical climates in both hemispheres (^{O´connor et al., 2006}), young animals and pregnant females are more susceptible to helminths as opposed to adult animals due to their nutritional status and low level of immunity (^{Vieira et al., 2014}). The prevalence of Haemonchus has been reported worldwide, in India ^{Tramboo et al. (2015)} out of a total of 1200 animals sampled 55 % were positive to the nematode; in Mexico, 32 % were found positive out of 219 sampled from grazing sheep (^{Hernández et al., 2007}); in the Sinaloa region when analyzing 120 sheep from an extensive production system a frequency of 17.5 % was reported (^{Gaxiola et al., 2010}). Therefore, the aim of this study was to determine the edaphoclimatic factors of different zones from Culiacán municipality and the production system that influence the prevalence of Haemonchus spp. in lambs in the central zone of Sinaloa.

MATERIAL AND MHETHODS

Type of study and sample size

This is an observational, cross-sectional, descriptive study. Twenty-three extensive, semi- intensive and intensive ranches were sampled. In the municipality of Culiacán, 125 Sheep Production Units (SPU) are registered (^{SIAP, 2013}), so the sample represented 18.4% of the SPUs. Ten of the 18 districts of Culiacán municipality, Sinaloa were considered (Figure. 1), the selection of the production units was made by convenience, based on the cooperation of the owner and ease of access. The sample size was determined with the following formula:

Figure 1 Location of the sheep production unit sampled in Culiacán Municipality, Sinaloa Mexico. 

n=Z2pqB2

Where: n is the sample size, Z is 1.96 for 95 % confidence, p is the expected frequency of the factor to be studied, q is 1-p, B is precision or admitted error (^{Jaramillo & Martínez, 2010}). The calculated sample size was 380 feces samples in each season (summer, fall, winter and spring) and because the number of lambs in the production unit was unknown at the time of the visit, the number of adults was considered (Table 1), and a number of lambs representing at least 10% of the adults in each production unit was sampled, which were randomly selected to complete the calculated sample size. Sampling was conducted by time of year and a total of 1520 samples were obtained from lambs less than ninety days (d) of age.

Table 1 Location of sheep production unit by district and population of adult sheep 

District	*SPU	Adult sheep	Lambs sampled
Villa Adolfo L.M	Agrícola Limón La Hacienda La granjita Alboradas	80 150 120 180	10 20 17 18
El Salado	El alacrán	70	11
Costa Rica	El trabajo Agrícola Sanfer Agrícola Tabachines	20 150 180	5 15 18
Quilá	Naranjos La Loma	70 30	12 5
Aguaruto	Fetasas Agrícola del Río Los Cabritos	200 45 200	22 5 20
Culiacancito	San Sebastián Agrícola Quiroz Los Otates	250 250 180	25 25 20
Las Tapias	Santa María	130	13
Sanalona	Baldomero	20	5
Imala	Guayacanes	200	24
Culiacán	Guásima Agrícola Mojolo Ganadera Verdugo Campo Morelia	230 300 80 180	23 32 15 20

*SPU= Sheep Production Units

RESULTS AND DISCUSSION

From a total of 1520 samples analyzed, 204 were positive for Haemonchus spp representing a prevalence of 13.42 % in the annual period analyzed; the method used to detect the nematode was the flotation technique, a test mainly used in stool examination in animal diagnosis, it concentrates eggs, parasite oocysts and separates the debris present in the sample (^{Zajac & Conboy, 2011}; ^{Rinaldi et al. 2011}; ^{Medeiros et al., 2018}), one of the main advantages of using this test is that it has a high egg recovery rate (^{Medeiros et al., 2018}), causes less damage to cysts and eggs (^{Zajac & Conboy, 2011}), which allows proper morphological identification facilitating the characteristic structure observation, egg dimensions to be identified (^{Indre et al., 2010}; ^{Mahmood et al., 2019}), the technique prevents flotation of trematode eggs and it is not as specific to determine the species of parasites observed (^{Zajac & Conboy, 2011}; ^{Ljungström et al., 2018}), therefore results using this technique report only the Haemonchus genus. Factors studied are presented in Table 2, Chi-Square tests indicated that the three factors were significant (P<0.05), year time, production zone, production system; similarly for the analysis of risk factors were significant (P≤0.05) in the multivariate logistic regression model (Table 3). The results by year time showed a higher prevalence in autumn with 20.53 %, no difference was observed between winter and spring and the lowest prevalence was found in summer with 7.89 % (P<0.0001).

The results of the study showed that when comparing the different seasons of the year, there is a 2.38 times higher risk of presenting Haemonchus spp. in autumn than in the rest of seasons (P<0.001). The results of the present investigation in relation to the summer season with 7.89 % are close to those described in England with 10.5 % (^{Broughan & Wall., 2007}), the low prevalence in summer can be attributed to the high temperatures that occur at this time in the area described, which is why the larvae decrease their activity, due to the negative phototropism to intense light (^{Soca et al., 2005}), in another study related to year times in India reported the presence of the order Strongylida with 63.2 % in summer and 58.4 % in autumn, 52.77 % in winter and 61.3 % in spring (^{Tramboo et al., 2015}), denoting difference with the current work, since in autumn there was a prevalence of 20.52 % being higher than that of summer with 7.89 %, this can be interpreted by the maximum temperatures that occur in summer in the study area, in addition to the increased humidity in the pastures in the autumn season that favor larval migration by positive hydrotropism (^{Soca et al., 2005}), regarding winter and spring, differences were also found between the two studies, since in India the prevalence increased from winter to spring, this is attributed to the precipitation that favors the humidity of the pastures for the presence of the parasite. Contrary to the present result, there was no significant difference from winter to spring in relation to the nematode presence, this is interpreted to the state of hypobiosis in which the helminth enters, in an unfavorable period nutritionally, so it tends to lower its metabolism and activity (^{Soca et al., 2005}); in a study conducted in Iran (^{Moghaddar, 2008}), sampled lambs under five months, during the four seasons of the year, it was reported the presence of nematodes 25.9, 22.3, 50 and 53.1 % for autumn, winter, spring and summer, respectively. The differences that stand out among the studies is the report of nematodes in general and therefore a higher percentage of positive lambs, another factor that indicates a difference between the prevalence between seasons is precipitation. In the case of Iran, there is more rainfall in March and April, so there are more nematodes in spring and summer, and in the study region of Culiacán, rainfall occurs in August and September, favoring the conditions for Haemonchus in autumn, coinciding with a study conducted in the same area with the protozoan Cryptosporidium spp. in lambs, showing 2. 2 times more risk of presenting the parasite in autumn than in summer (^{Castro et al., 2017}), although they are taxonomically classified in different phylum the climatic conditions at this time favor both.

When analyzing the geographic zone of the region, the results indicate a higher prevalence for the valley with 14.73 % as opposed to the highland zone with 3.83 % (P<0.0001), and 2.70 times higher risk of presenting the nematode in lambs in the valley zone (P<0.016). 016), presenting similarity to what was found in Ethiopia the difference that was reported in general were gastrointestinal nematodes, in valley production zone was higher than the high zone, with 95 and 68.6 % respectively and coincide in terms of higher risk of presenting Haemonchus in the valley production zone (^{Asmare et al., 2016}), likewise in Switzerland in high zones a low presence of the parasite was reported in comparison with medium and low zones in Italy and Ireland (^{Rinaldi et al., 2015}), the water source is one of the key characteristics for the survival and dissemination of nematodes such as Haemonchus (^{Musella et al., 2011}; ^{Rinaldi et al., 2015}), which occurred more in valley areas mainly because of dams, these areas are lower areas that can carry contaminants through water tributaries, including parasite eggs from production units or wild animals that live in higher areas, favoring the dissemination of these when this water is used for irrigation, animal consumption, among other activities of common use. Gastroenteric parasites and especially Haemonchus have managed to adapt to different ecosystems, their ability to adapt and survive different environments allow the infection of new hosts (^{Munguía et al., 2018}).

According to the production system the presence of Haemonchus spp was found 25.63% in extensive production system, 20.13 % in semi-intensive system and 5.03% in intensive system (P<0.0001) and when analyzing the association of parasitosis this was 4.81 times more risk of occurrence in lambs under an extensive production system (P<0.0001). The results differ from those performed by ^{Zapata et al. (2016)} and ^{Herrera et al. (2013)} in which no statistical difference was found among the three production systems analyzed. The conditions of the present study in animals under extensive systems are not systematized, they did not manage a deworming schedule, which agrees with ^{Mederos et al. (2010)} who indicate that the highest levels of gastrointestinal parasites occur in production units where there is no routine deworming management; in addition to the type of grazing-based feeding facilitates the ingestion of the parasite larvae present in the vegetation, and allows transmission as the animals themselves contaminate the grazing area (^{Belina et al., 2017}; ^{Akyüz et al., 2019}); on the other hand, in the semi- intensive and intensive systems, deworming management was programmed and feeding was operated with diets prepared mainly in the intensive system which favored a lower percentage of the parasite presence in these systems due to the positive impact given by better quality diets on health; ^{Cériac et al. (2019)} and ^{Naeem et al. (2021)} point out that quality nutrition supplemented with high protein, amino acids stimulates the expression of host resistance and resilience, stimulates immunity, decreases parasite proliferation.

CONCLUSION

The autumn season, valley area and extensive production system are the edaphoclimatic factors associated with the prevalence of Haemonchus spp (13.42%) in lambs in Culiacán municipality, Sinaloa; therefore, these aspects should be taken into account to develop strategies for the prevention and control of parasitosis. H. contortus is recognized as one of the main parasites affecting sheep, which makes it necessary to consider this agent as a possible cause of productive disorders even in early stages of the animals' age, as well as a possible infection source from young animals to the rest of the flock.