Cryptosporidium infection in cattle and sheep in central Oromia, Ethiopia

doi:10.21203/rs.3.rs-2009200/v1

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Cryptosporidium infection in cattle and sheep in central Oromia, Ethiopia

https://doi.org/10.21203/rs.3.rs-2009200/v1

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Background: Cryptosporidiosis is commonly caused by Cryptosporidium parvum and causes gastrointestinal illness in a wide variety of mammals including humans, cattle, sheep, goats, pigs and horses worldwide.

Methods: A cross sectional study was conducted from December 2021 to July 2022 to estimate the prevalence, identify associated risk factors and estimate infection intensity of the parasite in cattle and sheep in Central Oromia. Fecal flotation sheathers’ solution and modified acid fast technique were used to identify Cryptosporidium oocysts from fecal samples.

Results: Out of 687 fecal samples examined, 182 (34.2%) cattle and 30(19.4%) sheep were found to be infected with Cryptosporidium. There was a significant difference (P< 0.05) in the Cryptosporidium infection between age groups of cattle with higher prevalence in young (43.4%) than adult age group (28.4%). Similarly, there was a significant difference (P< 0.05) in Cryptosporidium infection among study sites. There was also a significant difference in Cryptosporidium infection between production systems with higher prevalence in intensive production system (38.7%) than the extensive system (21.6%). There was a significant difference in the intensity of infection of Cryptosporidium (P= 0.000) between the age groups of cattle with more burden of infection in the young age category than the adult age group.

Conclusion: The present study indicated that Cryptosporidium is widely distributed in cattle and sheep in the study areas. Significant number of adult animals were infected with this parasite indicating that adult animals could also play a great role in the parasite transmission. The majority of Cryptosporidium infections in both cattle and sheep were mild.

Cryptosporidium

Central Oromia

intensity of infection

risk factors

prevalence

Gastrointestinal parasites are considered as one of the most significant constraints in livestock sector. Damages inflicted to the health and productivity includes loss in body weight, poor reproductive performance, digestive disturbances, and emaciation for longer period [1]. It has been established that parasitic infections result in considerable losses in milk production in cattle [2]. Livestock carry large numbers of protozoa in their stomachs and intestines, the vast majority of which are entirely harmless. Some species of protozoa, however, are significant as causes of disease in domestic cattle, sheep and poultry, or because of their potential for zoonotic transmission [3].

Cryptosporidiosisis caused by a protozoan parasite of the genus Cryptosporidium, family of Cryptosporididae, Order Eucoccidiorida, class of Coccidia and phylum Apicomplexa. The parasite infects epithelial cells in the microvillus of gastrointestinal tract of all classes of vertebrates [4] and causes severe chronic and even fatal diarrhea with malabsorption and dehydration.

Currently, there are 26 Cryptosporidium species and more than 70 genotypes that are recognized as valid on the basis of morphological, biological and molecular data. The hosts ranges and pathogenicity is species variable. Among the species, Cryptosporidium parvum is the most common species of medical and veterinary importance. Most people and animals infected with Cryptosporidium parvum develop immunity and recover from that infection. However, the disease is persistent and life threatening if there is immunologic impairment [5].

Cryptosporidiosis in ruminants has a worldwide distribution. It has been documented in people and animals in 95 countries [6]. Most of the published reports were from Europe and little is known on the prevalence of ruminants’ Cryptosporidiosis in Africa. Study reports on the occurrence of Cryptosporidium in ruminants are very rare in Ethiopia. Some of the prevalence reports range from 7.2% to 18.6 % [7,8,9,10]. A wide-ranging study conducted in nine regions of the country reported an overall prevalence of 2.3% [11] while a study in eastern region reported a prevalence of 27.8% [12]. Molecular characterization of Cryptosporidium isolates from nine regions and central part of the country confirmed the existence of four species: C. parvum, C. andersoni, C. bovis and C. ryanae in the Ethiopian cattle [11, 12]. This indicates that there is few information on epidemiology, seasonal occurrence and intensity of Cryptosporidium infection in cattle and sheep in the study areas. Therefore, this study was initiated with the following objectives:

To estimate the prevalence of Cryptosporidium infections in cattle and sheep
To assess the seasonal dynamics of the parasite in cattle and sheep in central Oromia
To identify risk factors associated with the occurrence of the parasite
To estimate the intensity/burden of infections by the parasite

2.1 Description of study areas

The study was conducted in three selected areas of central Ethiopia namely Bishoftu (Mid land), Adama (Low land) and Holeta (High land) (Figure 1). Cattle and sheep managed under both intensive (Dairy farms) and extensive productions systems were considered for the study.

Bishoftu town is located at 9°N latitude and 40°E longitudes, 47 km south-east of Addis Ababa, at an elevation of 1850 meter above sea level. A bimodal rainfall pattern exists in the area, with a short rainy season from March to May and a longer wet season from June to September. It has an annual rainfall of 866mm of which 84% is in the long rainy season and the remaining in the short rainy season. The dry season extends from October to February. The area's average annual maximum and lowest temperatures are 26°C and 14°C, respectively, with a 61.3 percent relative humidity [13]. Farmers in the Bishoftu and its surroundings use mixed agricultural and livestock production. Furthermore, Bishoftu and its surroundings provide a diverse range of agro ecologies that are typical of the country. Different plant and animal species live in these agro-climatic zones. The livestock population on the basis of species is estimated to be 160,697 cattle; 22,181 sheep; 37,510 goats; 1,660 equines and 191,380 poultry [14].

Holeta is a town located in West Shoa Zone, Oromia region, Ethiopia, at a distance of 35 Km from Addis Ababa, lying between elevations of 2,320 and 2,460 meters above sea level. The average rainfall in Holeta is 1,367 mm and the mean temperature varies from 12.3 to 15.9 ^oc with a 9°15 N and longitude of 38°25'- 38°45' E. Human population in 2015 was estimated to be 57,828 with an average of 6.7 members per household. The area gets annual rain fall of 834-1300 mm and the annual temperature of 11-22°C. Rainy season occurs with bimodal distribution 70% of which occurs during the main rainy season (June to September) and 30% during the small rainy season (February to April) and relative humidity of 50.4% [13]. The main economic activity is agriculture with several crops cultivated in the area. Farming of livestock is rising and contributes to the development of the economy of the area as well. The town obtains grain products, livestock supply, natural resources and labour from surrounding areas and manufacturing and commercial products from Addis Ababa. The total cattle population of the study area is estimated to be 175,741, out of which 172,769 (98.3%) heads of cattle are local breeds and 2972 (1.7%) are crosses kept under extensive and semi intensive management systems, and the remaining are kept in intensive management system. Dairy farm is carried out in the area both in large scale dairy production system for commercial purpose and in smallholder farming system [15]

Adama is a city is located 95 km south eastern Addis Ababa 39.17°N and 8.33°E with an altitude of 1570 meter above sea level, latitude 8.31°N and 39.16°E longitude. Adama is situated in the well-known East African rift valley. It has annual rain fall temperature ranging from 400mm-800mm and 13.9°c-27.7°c, respectively [13]. The town is one of the most populous from the regional state and is located at an important multidirectional trade route. The numbers of livestock on the bases of species are 70, 662 cattle; 36, 142 sheep; 42, 968 goats; 31, 905 equines; 42 camels and 195, 155 poultry [16].

2.3 Study animals

Cattle of different breeds (Local, cross and exotic) and sheep were the study population of this study. Fecal samples were collected from five dairy farms (Three from Bishoftu, One from Holeta and one from Adama town) and from local cattle and sheep from three veterinary clinics. Production systems, animal species, breed, age, sex, study sites/farms, agro ecology, season of the year, body condition of the animals and fecal consistency were recorded during sampling. The study animals were categorized in to young and adult (For cattle, young refers to less two than years; adult is more than two years; for sheep young refers to less than one year and adult is more than one year) according to [17]. The body condition of cattle and sheep was categorized as poor, medium and good respectively as per the guide lines by [18] and [19].

2.3 Study design and sample size determination

A cross-sectional study design was employed for the study. Cluster sampling technique was used for the study involving dairy farms. Whereas, purposive sampling technique was used for collection of fecal samples from veterinary clinics. The desired sample size for the study was calculated using the formula given by [20] with 95% confidence interval and 5% absolute precision.

Where, Pexp = expected prevalence; d= absolute precision; N =sample size.

Considering 15.8 % expected prevalence of intestinal protozoal infections in cattle [9] in central Ethiopia, the sample size for one study animal species was 204. Since we considered two animal species (Cattle and sheep), the total sample size was calculated to be 204*2 = 408. However, we increased the sample size to 687 samples.

2.4 Sample collection and laboratory analysis

2.4.1 Coprological examination

About 10gram of fresh fecal samples were collected from cattle and sheep directly from the rectum using sterile disposable gloves. The samples were placed in labeled universal bottles, preserved in 10% formalin with the ratio of 1 gram of feces to 3 ml of formalin to prevent Cryptosporidium oocysts from desiccation, and transported in ice box to the parasitology laboratory of Addis Ababa University, College of Veterinary Medicine for laboratory analysis. Fecal flotation using concentrated sugar solution (sheathers’ solution) and Modified acid fast techniques were used to detect the oocysts of Cryptosporidium [8,10] A sample was considered positive for Cryptosporidium species if an oocyst of correct morphology was detected, i.e. optical properties, internal structure, size and shape as described by Fayer [21].

2.4.2 Determination of intensity of Cryptosporidium infection

The average number of oocysts in 10 randomly selected fields (oocyst per-field) of 100X magnification, was used to determine the intensity of Cryptosporidium oocysts. The intensity of oocyst was graded as: low (1–5 oocyst), medium (6–10 oocyst), and high (above 10 oocysts) [22].

2.5 Data management and statistical analysis

The statistical analysis was performed using SPSS 26 software. Chi square test and Manny-Whitney Test of non-parametric values were the statistical tests utilized to analyze the data. logistic regression analysis was also used to identify the potential risk factors associated with the occurrence of intestinal protozoal parasites at a desired precision level of 5 % and confidence interval of 95 %. Significant difference was considered when P< 0.05.

3.1. Cryptosporidium infections in cattle and sheep

Out of 687 fecal samples examined by coprology, 212 (30.9%) of cattle and sheep were found to be infected with Cryptosporidium. Statistically, there was a significant difference (P ˂ 0.05) in Cryptosporidium infection between the study animals with higher prevalence in cattle (34.2%) than sheep (19.4%) (Table 1).

Table 1

Over all prevalence of cryptosporidium infection in cattle and sheep
Animal species	Number of animals examined	Number positive (%)	X²	Odds ratio	95% C.I	P value
Cattle	532	182(34.2)	12.415	2.167	1.4-3.354	0.01*
Sheep	155	30(19.4)		0.24 (Ref)
Total	687	212(30.9)
* Significant difference

3.1.1. Cryptosporidium infections in cattle

Out of 532 fecal samples examined by coprology, 182 cattle (34.2%) were found to be positive for Cryptosporidium parasite. Univariate logistic regression analysis indicated that there was a significant difference (P < 0.05) in Cryptosporidium infections between age groups; among the different body conditions; among study sites/farms, between seasons; among agro - ecologies and between productions systems (Table 2). However, in multivariate logistic regression analysis of the data, only three risk factors namely age of the animals, the study sites/farms and the production systems were found to be associated with the occurrence of Cryptosporidium infections in cattle (Table 3).

Table 2

Univariate logistic regression analysis of the association between cattle Cryptosporidium infection and the hypothesized risk factors
Factors	Number of animals examined	Number positive (%)	X²	Odds ratio	95% C.I	P-value
Breed			4.049			0.132
Cross	12	5(41.7)		1.8	0.546–5.937
Exotic	344	127(36.9)
Local	176	50(28.4)		Ref.
Sex			0.913			0.339
Female	408	144(35.3)		1.234	0.801–1.902
Male	124	38(30.6)		Ref.
Age group			12.55			0.000*
Adult	327	93(28.4)		Ref.
Young	205	89(43.4)		2.767	0.359–3.747
Body condition			11.31
Good	299	120(40.1)		1.49	0.816–2.721	0.003*
Medium	175	44(25.1)
Poor	58	18(31)		Ref.
Study site/Farm			48.273			0.000*
Adama dairy farm	133	58(43.6)		2.033	0.97–4.16
Adama Vet clinic	36	5(13.9)		3.304	1.498–7.284
ARPC	63	35(55.6)		0.929	0.384–2.24
CVMA-VTH	50	13(26)		0.701	0.295–1.669
EMDI dairy farm	92	40(43.5)		2.044	1.011–4.1123
Holota dairy farm	45	4(8.9)		0.378
Holota vet clinic	62	13(21)		0.384
Tasew dairy farm	51	14(27.5)		Ref.
Season			19.979			0.000*
Dry	425	165(38.8)		3.36	1.931–5.84
Rainy	107	17(15.9)		Ref.
Agroecology			20.276			0.000*
High land	107	17(15.9)		0.285
Low land	169	63(37.3)		0.662
Mid land	256	102(39.8)		Ref.
Production system			13.331			0.000*
Extensive	139	30(21.6)		Ref.
Intensive	393	152(38.7)		0.631	0.278–0.686
Fecal consistency			1.562			0.462
Diarrheic	29	13(44.8)		1.638	0.741–3.623
Dry	319	108(33.9)
Moist	184	61(33.2)
Over all	532	182(34.2)

Note: * Significant difference;

CVMA: College of Veterinary medicine and agriculture; ARPC: Animal research and production center; VTH: Veterinary teaching hospital; EMDI: Ethiopian meat and dairy institute

Table 3

Multivariate logistic regression analysis of the association between cattle Cryptosporidium infection and the hypothesized risk factors
Factors	Number of animals examined	Number positive (%)	X²	Odds ratio	95% C.I	P-value
Age group			12.55			0.000*
Adult	327	93(28.4)		Ref.
Young	205	89(43.4)		2.767	0.359–3.747
Study sites/Farms			48.273			0.000*
Adama dairy farm	133	58(43.6)		2.033	0.97–4.16
Adama Vet clinic	36	5(13.9)		3.304	1.498–7.284
ARPC	63	35(55.6)		0.929	0.384–2.24
CVMA-VTH	50	13(26)		0.701	0.295–1.669
EMDI dairy farm	92	40(43.5)		2.044	1.011–4.1123
Holota dairy farm	45	4(8.9)		0.378
Holota vet clinic	62	13(21)		0.384
Tasew dairy farm	51	14(27.5)		0.426
Production system			13.331			0.000*
Extensive	139	30(21.6)		Ref.
Intensive	393	152(38.7)		1.631	0.278–0.286
Over all	532	182(34.2)
Note: * Significant difference; CVMA: College of Veterinary medicine and agriculture; ARPC: Animal research and production center; VTH: Veterinary teaching hospital; EMDI: Ethiopian meat and dairy institute

3.1.2. Cryptosporidium infections in sheep

From a total of 155 fecal samples examined through coprology, 30 sheep (19.4%) were infected with Cryptosporidium. Body condition was found to be the only risk factor associated with Cryptosporidium infection in sheep (Table 4).

Table 4

Univariate logistic regression analysis of the association between the different factors and *Cryptosporidium* infection in sheep
Factors	Number of animals examined	Number positive (%)	X²	Odds ratio	95% C.I	P value
Sex			2.756			0.097
Female	93	22(23.7)		2.092	0.865–5.097
Male	62	8(12.9)		Ref.
Age			0.095			0.758
Adult	112	21(18.8)		0.872	0.364–2.091
Young	43	9(20.9)		Ref.
Body condition			8.236			0.033*
Good	100	26(26)		8.081	1.039–62.859
Medium	31	3(9.7)		Ref.
Poor	24	1(4.2)
Season			0.000			0.988
Dry	119	23(19.3)
Rainy	36	7(19.4)
Agroecology			0.006			0.164
High land	36	7(19.4)		0.388	0.145–1.030
Low land	59	0(0)
Mid land	60	23(38.3)
Fecal consistency			1.527			0.986
Diarrheic	6	0(0)		0.000
Dry	138	28(20.3)		1.145	0.234–5.602
Moist	11	2(18.2)
Study site			28.006			0.164
Adama vet clinic	59	0(0)		0.000
CVMA- VTH	60	23(38.3)		2.575	0.971–6.833
Holota Vet clinic	36	7(19.4)
Over all	155	30(19.4)
Note: * Significant difference;
CVMA: College of Veterinary medicine and agriculture; VTH: Veterinary teaching hospital

3.2. Infection intensity/burden of Cryptosporidium parasite

The oocysts of Cryptosporidium were detected and semi quantitatively counted under the microscope based on their morphology (Fig. 4). The majority of Cryptosporidium infections in both cattle and sheep were mild. Low, Medium and high infection intensity in cattle was 37.4%, 26.9% and 33% respectively while low, medium and high infection intensity of Cryptosporidium in sheep was 60%, 20% and 23% respectively (Figs. 2 & 3).

3.3. Age related intensity of Cryptosporidium infection

There was a significant difference in the intensity of infection of Cryptosporidium (P = 0.000) between the age groups of cattle with more burden of infection in the young age category than the adult age group (Table 5). However, there was no significant difference (P > 0.05) in intensity of infection between the age groups in sheep.

Table 5

Manny-Whitney Test analysis of the association between intensity of Cryptosporidium infections and the age groups of cattle
Age group	Number examined	Mean Oocysts count of Cryptosporidium	Z- value	P -value
Adult	327	249.27	-3.896	0.000*
Young	205	293.99
Total	532
*Significant difference

During this study, the prevalence of Cryptosporidium in cattle was 34.2%. This finding is similar to the report of [23] (34.1%) from Kafre-Sheikh province and [24], (28.2%) from Mukure district of Kenya. The present record is lower than the finding of [25] who reported 64% prevalence from Brazil.

However, our finding was greater than the reports of authors from different regions of the Ethiopia: [26] (13%) from southern Ethiopia; [27] (18.6%) from North West Ethiopia; [8] (13.6%) from Bishoftu, Ethiopia; [9] (15.8%) from central Ethiopia; [28] (7.8%) from North Shewa and [10] (18.6%) from Addis Ababa, Ethiopia. The differences in the prevalence reports from different study areas could be attributed to the variation in climatic conditions, husbandry practices, the study methodologies employed and the age of the target population for the studies.

There was a significant difference in cattle Cryptosporidium infections between age groups of the animals with higher prevalence in young age group (43.4%) than adult age group (28.4%). This finding agrees with the reports of [25] and [27]2018; who reported high prevalence in young than adult age group. This could be related to the underdeveloped immune system of young age group which results in their higher susceptibility to Cryptosporidium infection [29]. However, the present result disagrees with the findings of [24] and [23] who reported insignificant difference in cattle Cryptosporidium infections between young and adult age groups.

The current 28.4% prevalence in adult age category indicates that adult cattle shed oocysts of Cryptosporidium and play a role in the parasite transmission through environmental contamination. This is supported by [29] who explained that adult cattle have a role in the outbreak of cryptosporidiosis in calves and humans, even though healthy calves under one month of age are the main carriers of Cryptosporidium parasite.

Similarly, there was a significant difference in cattle Cryptosporidium infections among the study sites/dairy farms with high prevalence in CVMA dairy farm (55.6%) than other dairy farms. There was also a significant difference in the infections between the two production systems with higher prevalence in intensive system (38.7%) than extensive production system (21.6%). This finding agrees with the report of [30], who registered a higher prevalence (42.8%) in intensively managed cattle than in extensively managed cattle. Our finding also agrees with the report of [10], who recorded high prevalence of Cryptosporidium infections (21.4%) in intensively managed cattle than those under the extensive system (11.2%). The difference in prevalence might be due to the difference in management systems in which the extensively reared cattle remain in large outdoor areas, reducing contact and oocyst contamination. In addition, cattle in extensive management systems have lower exposure to infection where oocysts are dispersed on a large surface and are exposed to direct sunlight, which reduces the oocysts' viability, resulting in a reduced infection pressure [31].

In this study, the prevalence of sheep Cryptosporidium infection was 19.4%. This finding is greater than the reports of [32] (1.4%) from France; [33] (11%) from Algeria; [34] (5.1%) from Greece; [35] (10.1%) from Poland; [17] (11.3%) from Iran and [22] (10.1%) from Italy.

Our finding however, is lower than the prevalence reports of [36] (29.06%) from Greece; [37] (28.7%) from Nigeria; [38] (28.5%) from China and [39] (30.6%) from California, USA. The low prevalence in sheep in this study could be due to the fact that fecal samples were collected from extensively managed animals which were kept out doors and were less exposed to Cryptosporidium oocyst than intensively managed sheep where overcrowding and confinement to small areas favor environmental contamination with oocysts and expose animals to infection [10]. Furthermore, in extensive management system, the oocysts are spread to large surface area resulting in low infection pressure [30].

The present findings in Cryptosporidium infections in cattle (34.2%) and in sheep (19.4%) could be a risk to public health, as Cryptosporidium is a zoonotic parasite particularly in immunologically compromised individuals. There was a significant difference in sheep Cryptosporidium infection among animals with different body conditions with high prevalence in animals with good body condition (26%) than medium (9.7%) and poor body condition (4. 2%).This finding seems to be a paradox and requires further detailed study. However, there was no significant difference observed in Cryptosporidium infections between age groups, sex, study sites, agro ecology, season of the year and fecal consistency in sheep.

The majority of Cryptosporidium infections in both cattle and sheep were mild. The current finding disagrees with the report of [10], who reported 44% of the positive samples to have more than 10 oocysts (High infection intensity) which is greater than our 33% of high infection intensity in cattle. This could be due to the fact that our samples were predominantly collected from adult animals as opposed to that of [10] who collected samples mainly from dairy calves and lambs.

The present study indicated that Cryptosporidium is widely distributed in cattle and sheep in the study areas. Significant number of adult animals were infected with this parasite indicating that adult animals could also play a great role in the parasite transmission through environmental contamination with oocysts of the parasite. There was a significant difference in the Cryptosporidium infection between age groups of cattle with high prevalence in young (43.4%) than adult age group (28.4%). Similarly, there was a significant difference in Cryptosporidium infection among study sites with higher prevalence in CVMA dairy farm (55.6%) than the rest of the study sites. There was also significant difference in Cryptosporidium infection between production systems with higher prevalence in intensive production system (38.7%) than the extensive system (21.6%).

Body condition was found to be the only risk factor associated with Cryptosporidium infection in sheep. There was no significant difference observed in Cryptosporidium infection between the dry and rainy season; among cattle breed and among the different fecal consistency in both cattle and sheep. The majority of Cryptosporidium infections in both cattle and sheep were found to be mild.

Based on the above conclusion, the following recommendations are forwarded:

Study on the economic impacts of Cryptosporidium parasite in ruminants should to be conducted
Detailed study on Cryptosporidium involving other domestic animals including pet animals should be initiated
Study on the pathogenic effects/pathology of Cryptosporidium should be conducted
Drug sensitivity trails on Cryptosporidium in domestic animals should be carried out
Study involving molecular method to identify the circulating species of Cryptosporidium in cattle and sheep should also be conducted

Ethics approval

The study protocol of Animal study has followed the guidelines of Addis Ababa University, College of veterinary medicine and Agriculture. The ethical clearance was reviewed and approved by Animal Research Ethical Review Committee of the college (Ref. No: VM/ERC/12/02/15/2022). Willingness of dairy farm owners and farmers were asked before the fecal sample collection from their animals.

Consent to publish

Not applicable (NA)

Availability of data and materials

The data and materials for the current study are available and can be obtained from the corresponding author.

Competing interests

There are no competing interests among the authors

Funding

No funding

Acknowledgements

We are highly indebted to dairy farm owners, veterinary clinics and farmers for allowing us to collect fecal samples.

Authors’ contributions:

The authors confirm contribution to the paper as follows:

Study conception and design: D A and BK

Data collection: DA and GA

Data analysis and interpretation, and draft manuscript preparation: DA and BK.

All authors reviewed the results and approved the final version of the manuscript.

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Cryptosporidium infection in cattle and sheep in central Oromia, Ethiopia

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Abstract

Figures

1. Introduction

2. Materials And Methods

3. Results

3.1. Cryptosporidium infections in cattle and sheep

3.1.1. Cryptosporidium infections in cattle

3.1.2. Cryptosporidium infections in sheep

3.2. Infection intensity/burden of Cryptosporidium parasite

4. Discussion

5. Conclusion And Recommendations

Declarations

References

Additional Declarations

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