Impact of environmental factors on Neospora caninum and Toxoplasma gondii infection in breeding ewes from western Mexico

doi:10.21203/rs.3.rs-3941635/v1

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Impact of environmental factors on Neospora caninum and Toxoplasma gondii infection in breeding ewes from western Mexico

https://doi.org/10.21203/rs.3.rs-3941635/v1

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Neospora caninum and Toxoplasma gondii are among the foremost causes of reproductive issues in sheep. The purpose of this study was to ascertain the influence of environmental factors associated with N. caninum and T. gondii infections in breeding ewes from western Mexico. A total of 184 blood samples were collected from breeding ewes to determine the seroprevalence of N. caninum and T. gondii using ELISA testing. With the seroprevalence data and information on the climatic and geographic conditions of the regions, environmental factors associated with N. caninum and T. gondii infections were identified through logistic regression analysis. A 15.21% of animals were found to have N. caninum antibodies (27/184), while a 61.9% prevalence (114/184) was observed in the case of T. gondii. The primary risk factors associated with N. caninum were Köppen climate area Ca(w1) with an odds ratio (OR) of 6.55 and Rainfall (700–800 mm) with an OR of 3.23. In the diagnosis of T. gondii, 113 positive sheep out of 184 included in the study were identified. In the risk analysis for T. gondii, the main risk factors observed were Köppen climate area Cb(w1) with an OR of 10.5 and Rainfall (900–1000 mm) with an OR of 4.6.

Sheep

Risk factors

Climate

Protozoa

Altitude

Soil

Neospora caninum is an apicomplexan protozoan with an indirect life cycle. warm-blooded animals such as cattle and sheep can serve as intermediate hosts, whereas dogs, coyotes, dingoes, and gray wolves have been identified as definitive hosts. N. caninum causes neurological issues in canines and reproductive problems in definitive and intermediate hosts (Dubey et al. 2011; Dubey et al. 2017; Lindsay et al. 2020).

On the other hand, Toxoplasma gondii is an intracellular parasite that can affect a wide range of warm-blooded species. Domestic and wild felines have been identified as definitive hosts, while various domestic animals such as birds, cattle, pigs, goats, and sheep are considered intermediate hosts. Transmission of T. gondii can occur through the ingestion of food and water contaminated with oocysts or through congenital transmission. The primary infection route in definitive hosts is oral, through the consumption of meat contaminated with tissue cysts (Dubey et al. 2017; Dubey 2021). Risk factors associated with N. caninum and T. gondii infection have been identified within sheep farms in western Mexico, including poor hygiene conditions, presence of definitive hosts, presence of other domestic animals, public water supply, among others (Alcalá et al. 2022).

Environmental factors influence the distribution of parasites such as N. caninum and T. gondii, as they can promote their development and performance. It has been reported that rainfall is associated with the contamination of infective stages of these parasites in water sources and animal grazing areas (Skuce et al. 2013). The ability of these parasites to adapt to their environment may reduce the negative impact on their life cycle and infectivity, thus favoring their persistence in the environment. It is essential to understand and identify the environmental factors that facilitate the development of various organisms, such as protozoa, and host-parasite interactions (Aleuy and Kutz, 2020).

It is important to identify environmental factors that favor the development and spread of parasites such as N. caninum and T. gondii, as understanding them will lead to a better comprehension of the environmental dynamics associated with the health-disease process. Additionally, it will enable the establishment of management and improvement programs in sheep farms, allowing for the maintenance of productive and economic parameters.

The aim of this study was to identify the impact of environmental factors associated with N. caninum and T. gondii infection in reproductive ewes in western Mexico.

Study site

The study was conducted in the state of Jalisco, located in the central-western region of Mexico. It has an average altitude of 1540 meters above sea level and an average temperature of 20.5°C. The region exhibits a range of climates, from warm subhumid to dry and semiarid. In the present study, the municipalities of Ixtlahuacán del Río, La Barca, Tepatitlán de Morelos, Tlajomulco de Zúñiga, Yahualica de González Gallo, and Zapopan were included.

Farms

Eight farms were selected, each assigned an identification code, distributed as follows by municipality (Fig. 1): Ixtlahuacán del Río: F1 (21° 03' 48" N, 103° 09' 03" W) and F2 (20° 54' 58.75" N, 103° 14' 13.16" W). La Barca: F3 (20° 16' 15" N, 102° 35' 54" W). Tepatitlán de Morelos: F4 (20° 55' 46" N, 102° 52' 02" W). Tlajomulco de Zúñiga: F5 (20° 27' 13" N, 103° 26' 18" W) and F6 (20° 29' 54.69" N, 103° 34' 30.95" W). Yahualica de González Gallo: F7 (21° 10' 06" N, 102° 50' 05" W). Zapopan: F8 (20° 47' 14.6" N, 103° 25' 30.76" W). All the farms have a grazing system supplemented with balanced feed. The animals exhibit a biotype characterized by a mixture of multiple hair breeds, with reproductive management based on direct mating.

Sampling

A sample size of 184 animals was determined using EpiInfo 7 software (Stata Corp. 2007). For this, the total population of registered reproductive ewes in the municipalities included in the study was considered, based on data from the National Livestock Registry (PGN, 2018). A 5-milliliter blood sample per animal was collected through venipuncture of the jugular vein, using new Vacutainer tubes without anticoagulant. The blood samples were transported to the laboratory and centrifuged (1000 g/15 min). After centrifugation, the sera were transferred to 2.5 ml plastic tubes and stored at -20°C until use.

Environmental factors

The environmental factors considered the following variables (Table 1): altitude, climatic classification, soil type, average annual precipitation, mean temperature, maximum temperature, and minimum temperature. During the sample collection visit, the geographical coordinates of each farm and the altitude above sea level were recorded. The climate type for each farm was determined using Köppen-García climate maps for Jalisco (Ruíz-Corral et al. 2021). Different soil types were obtained from digital soil maps developed by the National Institute of Statistics and Geography (INEGI) (INEGI, 2023). To obtain the average annual precipitation, mean temperature, maximum temperature, and minimum temperature, climate databases for each of the municipalities included in the study were analyzed (SMN, 2023). Daily data from eight weather stations, managed by the Comisión Nacional del Agua (CONAGUA), were utilized. The stations were selected based on their proximity to the farms included in the study. A historical data series from the period 1998–2018 was analyzed.

Table 1

Environmental parameters considered for risk analysis
Farm	Municipality	Altitude*	Köppen climate area	Soil type	Mean annual rainfall	Annual mean temperature	Maximum temperature	Minimum temperature
F1	Ixtlahuacán del Rio	1509	Ca(w1)	Phaeozem	839.54 mm	18.28 ºC	39.5 ºC	-5.5 ºC
F2	Ixtlahuacán del Rio	1829	Ca(w1)	Phaeozem	839.54 mm	18.28 ºC	39.5 ºC	-5.5 ºC
F3	La Barca	1530	(A)Ca(w1)	Vertisol	901.64 mm	20.42 ºC	39.5 ºC	-3 ºC
F4	Tepatitlán de Morelos	1655	Cb(w1)	Phaeozem	859.32 mm	18.6 ºC	36.5 ºC	-6 ºC
F5	Tlajomulco de Zúñiga	1560	(A)Ca(w1)	Andosol	944.72 mm	18.68 ºC	43.5 ºC	-5.5 ºC
F6	Tlajomulco de Zúñiga	1493	(A)Ca(w1)	Andosol	944.72 mm	18.68 ºC	43.5 ºC	-5.5 ºC
F7	Yahualica de González Gallo	1806	(A)Ca(w1)	Phaeozem	733.41 mm	18 ºC	39 ºC	-10 ºC
F8	Zapopan	1594	Ca(w1)	Regosol	1009.55 mm	20.65 ºC	39.5 ºC	0 ºC
* Meters above sea level (masl)

Serological tests

To determine the presence of IgG antibodies against N. caninum, serum samples were subjected to an indirect ELISA using the commercial IDEXX Neospora Ab Test kit (IDEXX Laboratories, Inc., Westbrook, Maine). Following the manufacturer's recommendations, the serum was diluted at a 1:100 ratio. Plate readings were performed at an optical density of 650 nm, with a cutoff point set at > 0.50. Positive and negative cases were determined using the xChekPlus software (IDEXX Laboratories, Inc., Westbrook, Maine).

The seroprevalence associated with T. gondii was determined using the commercial IDEXX Toxotest Ab Test kit (IDEXX Laboratories, Inc., Westbrook, Maine). Serum samples were diluted at a 1:400 ratio following the manufacturer's recommendations. Plate readings were conducted at an optical density of 450 nm, with a cutoff point set at > 0.30. Positive and negative cases were determined using the xChekPlus software (IDEXX Laboratories, Inc., Westbrook, Maine).

Data analysis

The data obtained were analyzed using logistic regression (Hosmer et al. 2013). The result of the serological tests was used as the dependent variable. Independent variables were determined using a backward stepwise method. The relationship of environmental factors was estimated through Odds Ratios (OR) and a 95% Confidence Interval (CI), with values greater than 1 indicating an association between variables. All collected data were analyzed using the Statistical Software Science System (STATA) v. 10.1 (StataCorp. 2007). P values < 0.05 were considered statistically significant.

Antibodies against N. caninum were detected in 28 out of 184 sheep. As part of the risk analysis and seroprevalence associated with N. caninum (Table 2), the following factors were identified: Altitude 1500–1600 masl, Köppen climate classification Ca(w1), soil type, Precipitation 700–800 mm, and mean temperature 18–19°C. The factors with the highest prevalence and risks were precipitation (seroprevalence 16.67%, OR 3.23; 95% CI 0.5–19.8), Köppen climate area Ca(w1) (seroprevalence 27.71%, OR 6.55; 95% CI 1.4–29.3; furthermore, this latter factor exhibited a statistically significant value of P < 0.05.

Table 2

Risk factors environmental associated with the presence of *N. caninum* in sheep herds in Jalisco, Mexico
Variable	Seroprevalence	OR*	95% C.I.*	P-value
Altitude 1500–1600 (masl)*	16.28	1.02	0.2–4.4	0.977
Köppen climate area Ca(w1) *	27.71	6.55	1.4–29.3	0.014
Soil type (vertisol)	13.89	2.90	0.4–20.4	0.271
Rainfall (700–800 mm)	16.67	3.23	0.5–19.8	0.206
Temperature medium (18–19 ºC)	13.98	1.16	0.2–4.8	0.838
^* OR = Odds Ratio; C.I. = Confidence Interval; Ca(w1) = Temperate with warm summer; summer rains; masl = Meters above sea level

In the case of T. gondii, infection was detected in 113 animals. The analysis of environmental risk factors (Table 3) reveals the following variables as risks: Altitude 1800–1900 masl, Köppen climate classification Cb(w1), soil type, precipitation 900–1000 mm, mean temperature 18–19°C, and minimum temperature − 5 - -3°C. It was observed that the Köppen climate area Cb(w1) variable showed the highest prevalence and risk (seroprevalence 95.65%, OR 10.5; 95% CI 1.8–60.4), while in the 900–1000 mm precipitation category, a seroprevalence of 56.30% was noted, with an OR of 4.6; 95% CI 1.1–18.2. In both cases, a statistically significant value of P < 0.05 is evident.

Table 3

Risk factors environmental associated with the presence of *T. gondii* in sheep herds in Jalisco, Mexico
Variable	Seroprevalence	OR*	95% C.I.*	P-value
Altitude 1800–1900 (masl)*	65.38	3	0.4–19.5	0.251
Köppen climate area Cb(w1) *	95.65	10.5	1.8–60.4	0.008
Soil type (regosol)	57.89	1.62	0.5–4.5	0.352
Rainfall (900–1000 mm)	56.30	4.6	1.1–18.2	0.030
Temperature medium (18–19 ºC)	75.27	2.84	0.3–24.3	0.339
Temperature minimum (-5- -3 ºC)	57.89	1.90	0.2–12.2	0.68
^* OR = Odds Ratio; C.I. = Confidence Interval; Cb(w1) = Temperate with long cool summer; summer rains; masl = Meters above sea level

In the present study, the association between various environmental factors and the infection of N. caninum and T. gondii in reproductive ewes in western Mexico was determined. This research allowed us to identify climatic zones that facilitate the spread of these protozoa. N. caninum shares similarities with T. gondii, and as a result, there is limited information regarding the environmental conditions favoring their development. Dubey et al. (2007) mention that the environmental resistance conditions for N. caninum are similar to those of T. gondii; however, this study identified different environmental conditions for each parasite. López-Gatius et al. (2005) note an association between rainfall and N. caninum associated abortions, identifying this parameter as a risk factor. On the other hand, Gazzonis et al. (2019), in a study conducted in northern Italy, identified annual mean temperature and annual precipitation as risk factors associated with N. caninum. This information aligns with the data observed in this research, where rainfall (700–800 mm) is a significant risk factor (OR 3.23), as well as mean temperature (18–19°C) (OR 1.16). Furthermore, Rinaldi et al. (2004) highlight the association between the presence of N. caninum in grazing areas and its relationship with environmental variables such as elevation, average annual precipitation, and mean temperature, which were identified as important risk factors in our study.

The identification of climatic regions where herds are located is crucial, as these can be considered a significant risk factor for N. caninum infection. In a study conducted in Portugal by Waap et al. (2022), they mention that climate types according to Köppen classification (Csa: hot summer Mediterranean climate and Csb: warm summer Mediterranean climate) are important risk factors. This aligns with the data presented in this study, where the Ca(w1) climate (temperate with warm summer; summer rains) was the highest-risk factor (OR 6.55). The similarities between both studies may be linked to the prevailing warm conditions in the areas, which can favor the survival and sporulation of N. caninum oocysts in the environment (Goodswen et al. 2012). Therefore, N. caninum prevalence can be associated with various ecological and geographic conditions characterizing the regions where herds are located (Nie et al. 2019; Selim et al. 2021; Fereig et al. 2022).

T. gondii cysts can survive adverse environmental conditions, including low temperatures. Kotula et al. (1991) mention the resistance capacity of infective stages to temperatures below − 12.4°C. However, the strains of T. gondii can vary in their ability to resist and remain infectious at temperatures as low as -37.5°C. This corresponds to the identification of the minimum temperature recorded during our study (-5 – -3°C), making it a significant risk factor (OR 1.90). On the other hand, the annual mean temperature is another crucial factor associated with T. gondii. Studies conducted by Alvarado-Esquivel et al. (2013), Stelzer et al. (2019), and Gazzonis et al. (2019) report that average temperatures not exceeding 20°C can favor the survival, viability, and infectivity of T. gondii oocysts. These findings align with the data observed in our study, where the recorded mean temperature was 18–19°C; hence, we identify it as a risk factor for the study area (OR 2.84). Our results are very similar to those reported by Gazzonis et al. (2019), as the risk value obtained in this same variable was an OR of 2.27.

In the case of rainfall, several authors indicate a direct association with the presence of T. gondii in herds (Stelzer et al. 2019; Gazzonis et al. 2019). On the other hand, other authors (Alvarado-Esquivel et al. 2013) mention that an annual precipitation exceeding 600 mm is associated with high seroprevalence of T. gondii in sheep. This research aligns with the results observed in the present study, where rainfall in the range of 900–1000 mm was one of the main risk factors obtained (OR 4.6), with statistical significance (P < 0.05). Meerburg and Kijlstra (2009) state that due to increased rainfall, T. gondii oocysts can spread more efficiently in the environment.

The predominant climate type in areas where herds graze can influence the presence and spread of infective stages of T. gondii (Stelzer et al. 2019). The classification of climatic zones is a tool that can help us establish a relationship between environmental variables and their association with parasitic diseases. In the present research, the climatic areas classified as Köppen climate area Cb(w1) were identified as one of the main risk factors for the presence and spread of T. gondii (OR 10.5, P < 0.05). A study conducted by Rodríguez-Ponce et al. (2016) describes that temperate climatic areas show an associated risk with T. gondii. Similarly, Yan et al. (2016) mention that climatic zones can influence the survival, distribution, and transmission of T. gondii.

Altitude is another factor that can favor the development of diseases such as toxoplasmosis in sheep (Caballero-Ortega et al. 2008; Stelzer et al. 2019). The research conducted by Alvarado-Esquivel et al. (2013) indicates that altitudes below 1900 meter above sea level masl are associated with high seroprevalence in sheep. These data align with what is reported in this study, where altitudes of 1800–1900 meters above sea level show a risk related to the presence of T. gondii (OR 3). On the other hand, it has been recognized that the soil type classified as regosol is associated with T. gondii (OR 1.62). Regosols are characterized by being young soils that result from erosion, where stones and sand are moved by water (Gargiulo et al. 2016). These soil movements associated with rainfall promote the dispersion of T. gondii oocysts more effectively (Meerburg and Kijlstra, 2009).

In conclusion, we can consider that N. caninum and T. gondii exhibit a significant relationship with environmental factors in western Mexico, with the most significant factors for both parasites being Köppen climate area Ca(w1) and Cb(w1), as well as rainfall. The identification of abiotic parameters associated with N. caninum and T. gondii can assist in herd management to reduce prevalence and minimize the economic losses they may cause.

Acknowledgements

We appreciate the support received from the Tecnológico Nacional de México, Instituto Tecnológico El Llano Aguascalientes, Universidad Autónoma de Guadalajara, and the owners of the sheep farms that participated in the study.

Author contribution

Conceptualization Jaime Alcalá-Gómez, and Leticia Medina-Esparza; methodology: Jaime Alcalá-Gómez, Leticia Medina-Esparza, Teódulo Quezada-Tristán and Gabriela Alcalá-Gómez; formal analysis: Jaime Alcalá-Gómez, Leticia Medina-Esparza, Teódulo Quezada-Tristán and Gabriela Alcalá-Gómez; writing-original draft preparation: Jaime Alcalá-Gómez, and Teódulo Quezada-Tristán; writing-review and editing Jaime Alcalá-Gómez, Leticia Medina-Esparza and Teódulo Quezad-Tristán All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Tecnológico Nacional de México, Instituto Tecnológico El Llano Aguascalientes through internal research grant SN/2020.

Data availability

Not applicable.

Code availability

Not applicable.

Ethics approval

The Committee on the Use and Care of Animals of the Instituto Tecnológico El Llano Aguascalientes and the farm owners approved this project (ITEL-CUCA 011/20).

Consent to participate

Authors have permission to participate.

Consent for publication

Authors have permission for publication.

Conflict of interest

The authors declare no competing interests.

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Impact of environmental factors on Neospora caninum and Toxoplasma gondii infection in breeding ewes from western Mexico

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Abstract

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INTRODUCTION

MATERIALS AND METHODS

Study site

Farms

Sampling

Environmental factors

Serological tests

Data analysis

RESULTS

DISCUSSION

Declarations

References

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