PREVALENCE OF GASTROINTESTINAL PARASITES, ANTHELMINTIC USE AND RESISTANCE IN SELECTED SHEEP FARMS

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ABSTRACT

The adverse effects of gastrointestinal parasitic infection have resulted in low productivity of sheep in Kenya. As a result, farmers relied on anthelmintic therapy that may lead to occurrence of anthelmintic resistance. The occurrence of clinical and sub-clinical cases despite treatment, enhanced the need to determine prevalence and intensity of gastrointestinal parasites infection in sheep, assess knowledge, practice and attitudes towards treatment and control of helminthes infection in sheep and test for anthelmintic resistance.
A cross-sectional study was conducted in 30 selected sheep farms in Kasarani to determine the prevalence and intensity of gastrointestinal parasites in different breeds of sheep. One thousand six hundred and forty-two (1642) faecal samples were subjected to coprological examination to determine the egg per gram (EPG), oocyst per gram (OPG) of faeces with a detection level of 100 EPG/OPG and for the presence of cestode and trematode eggs. The overall prevalence of gastrointestinal parasites was 99.6 %. The prevalence of strongyle eggs was 72%, coccidial oocyst 49% and 7% for tapeworm eggs. There was no significant difference in prevalence of strongyle between adults and lambs (P-value 0.7), males and females (P value 0.4) and coccidial infection between adults and lambs (P value 0.2) and male and female (P value 0.3). Prevalence of tapeworm infection in between adults and lambs (P-value 0.000) and male and female (P value 0.0001).
The overall intensity of strongyle (480 mean egg count (MEC) and coccidial (330 mean oocyst count (MOC) infection in sheep were low. At farm level the intensity of strongyle (32-1561 MEC) and coccidia (7-2034 MOC) ranged from mild to severe (MEC, 2034 MOC). Helminthes spectrum showed 90% Haemonchus species, 5% Trichostrongylus species and 5% Oesophagostomum species. There was no evidence of trematode infection in the sampled sheep. 
Survey on knowledge, practice and attitude towards treatment and control of gastrointestinal parasites showed that all the respondents 77(100%) were aware about helminthes infection in sheep. Classes of anthelmintics available in veterinary drugs stores were benzimidazole, imidazothiazole and macrocyclic lactones. The proportions of farmers using these anthelmintics were 43%, 30% and 27% respectively. The ease of administration (70%) and price (30%) greatly influenced the choice of anthelmintics to use. Veterinary consultation was rare (13%) in suspected case of sheep helminthosis. Dose determination was based on visual estimation of the sheep’s weight (67%) and weight of individual sheep (33%). Deworming was done every three months (67%) and whenever there was sign of helminthes infection (33%). In every subsequent treatment a different class of anthelmintics was used (73%).
Faecal egg count reduction test (FECRT) detected multiple anthelmintic resistance whereby resistance to albendazole, levamisole and ivermectin was confirmed in one farm with FECR% of 11.1%, 59.3%, 59.3% respectively. More farms (60%) showed resistance to albendazole than to levamisole (40%) and ivermectin (40%). Haemonchus contortus and Trichostrongylus species were resistant to the three anthelmintics while Oesophagostomum species were resistant to levamisole and ivermectin.
This study demonstrated high prevalence of 99.6% of gastrointestinal parasites infection in sheep. The inappropriate dosing, frequent deworming and short alternation period might have resulted in occurrence of multiple and multi-generic anthelmintic resistance (AR) in sheep in Kasarani Sub- County. Therefore, there is need to educate farmers on proper use of anthelmintics, the risk of anthelmintic resistance occurrence and its consequences on production.



 
TABLE OF CONTENTS
 
DECLARATION ii
DEDICATION iii
ACKNOWLEDGEMENT iv
TABLE OF CONTENTS v
LIST TABLES x
LIST OF FIGURES xi
LIST OF APPENDICES xii
ABSTRACT xiii

CHAPTER 1: INTRODUCTION AND OBJECTIVES
1.0 INTRODUCTION 1
1.1 OBJECTIVE 3
1.2 SPECIFIC OBJECTIVES 3
1.3 RESEARCH QUESTIONS 3
1.4 HYPOTHESIS 3
1.5 JUSTIFICATION 3

CHAPTER 2: LITERATURE REVIEW
2.1 Sheep Farming Systems 5
2.1.1 Extensive Production System 5
2.1.2 Intensive Production System 5
2.1.3 Traditional Pastoralism Production System 5
2.2 Parasitism in Sheep 7
2.3 Gastrointestinal parasites of sheep 7
2.3.1 Helminthes parasites of sheep 7
2.3.1.1 Factors that influence level of host infection 8
2.3.1.2 Nematode Life Cycle 9
2.3.1.3 Effect and clinical signs of GI nematode infection 10
2.3.1.4 Life cycle of sheep’s trematode 11
2.3.1.5 Life Cycle of Paraphistomes spp 12
2.3.1.6 Life Cycle of Sheep’s Cestodes 12
2.3.1.7 Diagnosis of helminthes 13
2.3.2 Sheep coccidiosis 14
2.3.2.1 Life cycle of coccidia 14
2.3.2.2 Clinical signs of coccidiosis 15
2.3.3 Prevalence of gastrointestinal parasites 16
2.4 Control of gastrointestinal parasites 17
2.4.1 Control of helminthes 17
2.4.1.1 Control by anthelmintic treatment 18
2.4.1.2 Pasture management 20
2.4.1.3 Breeding for genetic resistance 21
2.4.1.4 Vaccination 21
2.4.1.5 Biological control 21
2.4.2 Control of Coccidiosis 21
2.4.3 Host immunity 22
2.4.3.1 The manifestation of immune competence includes 22
2.5 Anthelmintic resistance (AR) occurrence and its detection/testing 23
2.5.1 Anthelmintic resistance occurrence 23
2.5.2 Anthelmintic resistance testing 23
2.5.2.1 In_vivo test diagnostic method 24
2.5.2.1.1 Faecal egg count reduction test (FECRT) 24
2.5.2.1.2 Controlled test 27
2.5.3.1 In_vitro diagnostic methods 27
2.5.3.1.1 Egg hatch Assay 28
2.5.3.1.2 Larval paralysis and motility Assay 28
2.5.3.1.3 Larval development assay 29
2.5.3.1.4 Tubulin binding Assay 29
2.5.3.1.5 Adult Development Assay 30
2.5.3.1.6 Micro-agar development test (MALDT) 30
2.5.4.1 Molecular based test 30
2.6 Control of Anthelmintics Resistance 31

3.0  CHAPTER 3: MATERIALS AND METHOD
3.1 Study area 32
3.2 Study design 32
3.3 Farm selection 32
3.4 Study animals 33
3.5 Data collection 34
3.5.1 Objective 1: Prevalence of gastrointestinal parasites 34
3.5.1.1 Collection of faecal samples 34
3.5.1.2 Modified McMaster technique 34
3.5.1.3 Sedimentation technique 35
3.5.1.4 Faecal Culture 35
3.5.2 Objective 2: Knowledge, practice and attitude survey 36
3.5.3 Objective 3: Investigation of anthelmintic resistance 36
3.5.3.1 Farm and animal selection 36
3.5.3.2 Anthelmintics administration 36
3.5.3.3 Faecal sample collection 37
3.5.3.4 Faecal sample analysis 37
3.6 Statistical analysis of data 37
3.6.1 Prevalence, Intensity and Spectrum 37
3.6.2 Questionnaires survey 38
3.6.3 Faecal egg count test (FECRT) data analysis and interpretation 38

4.0  CHAPTER 4: RESULTS
4.1 Prevalence of GI parasites in sheep in Kasarani Sub-County, August 2021. 41
4.1.3 Prevalence of GI parasites by age group and sex in Kasarani Sub-County, August 2021. 42
4.2 Intensity of Gastrointestinal parasites in sheep in Kasarani Sub-County 42
4.2.1 Intensity of GI parasites infection in different ages and sexes of sheep. 43
4.3 Helminthes spectrum 44
4.3.1 Parasites Observed 44
4.3.2 Larval stage three identified 46
4.4 Knowledge, practice and attitude survey-questionnaire results 48
4.5. Anthelmintic Resistance 51

5.0 CHAPTER 5 
DISCUSSION

6.0 CHAPTER 6
CONCLUSION AND RECOMMENDATION 59
REFERENCES 61
APPENDICES 73



 
LIST TABLES

Table 2.1: In_vitro AR diagnostic tests and respective anthelmintics they test 27
Table 3.2: Classes of anthelmintics drugs, dosage rate and route of administration used for FECRT, with their respective treatment groups (animal groups) 36
Table 4.1: Prevalence of GI parasites infection in different age groups and sexes in Kasarani Sub- County, August 2021. 42
Table 4.2: Intensity of GI parasites infection in different ages and sexes of sheep in Kasarani Sub- County, August 2021. 43
Table 4.3:Categories of respondents on Knowledge, Practice and Attitude (KPA) towards diagnosis, treatment and control of helminthes in sheep in Kasarani Sub-County, August 2021 49
Table 4.4: Farmers’ Knowledge, Practice and Attitude (KPA) towards diagnosis, treatment and control of helminthes infection in sheep in Kasarani Sub-County, August 2021 Error!
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Table 4.5: Percentage Faecal Egg Count Reduction (FECR%) and Lower 95% Confidence Level (CL) for the anthelmintics drugs tested for resistance in the selected 10 farms in Kasarani Sub-County 52
Table 4.6: The overall percentage differential counts of L3 identified in the treated and control groups 54
Table 4.7: Number of farms showing helminthes genera resistance to the tested anthelmintics 54
 




LIST OF FIGURES
Figure 3.1: A Sketch of map of Kenya showing location of Kasarani Sub-County in Nairobi County. Source; (Google Map) 33
Figure 4.1: Overall prevalence of GI parasite infection in sheep in Kasarani Sub-County, August 2021. 41
Figure 4.2: Overall intensity of GI parasites infection in sheep in Kasarani Sub-County, August 2021. 43
Figure 4. 3 (a) and (b): Strongyle egg at x10 and at x 40 magnification 45
Figure 4.4 (a) and (b): Tapeworm and strongyle eggs at x10 and at x40 magnification 45
Figure 4. 5 (a) and (b): Coccidial oocyst and strongyle egg at x10 and at x40 magnification 45
Figure 4. 6: Overall helminth spectrum in sheep in Kasarani Sub-County, August 2021. 46
Figure 4.7: Helminthes spectrum at farm level in Kasarani Sub-County, August 2021. 47
Figure 4. 8 (a) and (b): Anterior and posterior end of Haemonchus contortus 48
Figure 4. 9 (a) and (b): Anterior and posterior ends of Oesophagostomum 48
Figure 4. 10 (a) and (b): Anterior and posterior ends of Trichostrongylus 48
Figure 4.11: Summary of the number of farms where resistance was confirmed and suspected 52



 
LIST OF APPENDICES
Appendix 1: KPA survey to agricultural and veterinary drug stores sales persons in Kasarani. .. 73
Appendix 2: a survey questionnaire on knowledge, practice and attitude towards treatment and control of gastrointestinal parasites in sheep, to farmers 75
Appendix 3: A survey questionnaire on knowledge, practice and attitude towards treatment and control of gastrointestinal parasites of sheep, for veterinary service providers in Kasarani 78
Appendix 4: List of farmers interviewed in KPA survey, their gender, farm location and flock size in Kasarani 80
Appendix 5: List of Agricultural and veterinary drug stores sampled in KPA, their location and duration of service in Kasarani 81
Appendix 6: List of Veterinary service providers interviewed in KPA survey, their biodata and location of practice in Kasarani 82
Appendix 7: Responses on Knowledge, Practice and Attitude towards treatment and control of helminthes in sheep by farmers in Kasarani 83
Appendix 9: Responses on Knowledge, Practice and Attitude towards sheep’s helminthes, treatment and control by veterinary service providers in Kasarani 88
Appendix 10: Prevalence of gastro-intestinal parasites infection in sheep in the selected 30 farms in Kasarani 91
Appendix12: Sheep’s helminthes genera identified in the selected 30 farms in Kasarani 94
Appendix 13: Percentage differential counts of L3 identified in the treated and control groups per farm in Kasarani 95




 
CHAPTER 1
INTRODUCTION AND OBJECTIVES

1.0 INTRODUCTION

Sheep have a high potential to affect the socio-economic growth of most African rural communities. Improving sheep production can increase farmers’ income, ability to acquire more inputs for other production activities, hence improved standard of living. Sheep of different breeds are mainly kept for mutton, milk, wool or dual purpose. Common breeds suitable for different regions in Kenya include: Merino, Hampshire down and Corriedale that are kept in high altitude areas; East African fat tailed type and dorper that are kept in medium altitude areas. East African fat-ramped type is kept in both high and medium altitude areas while red Maasai, dorper and Persian black head are kept in low altitude areas (Baker et al, 2002).
Sheep population in the world is approximately 1.2 billion (Mazinani and Rude 2020). In Africa sheep population is 352 million representing 30% of the world’s population of small ruminants (Mazinani and Rude 2020). Kenya’s small ruminant population is estimated to be 46 million out of which 42% are sheep (FAOSTAT, 2020). The livestock sector in Kenya is a source of livelihood to rural and urban population and contributes 12% of Gross Domestic Product (GDP) (Ministry Livestock and Fisheries, 2008). In Nairobi, 10% of the livestock population are small ruminants consisting of approximately 4%, sheep. In Kasarani Sub-County 3% of the livestock population are sheep (KBS, 2019).
In arid and semi-arid land (ASALS) livestock production industry is estimated to contribute 90% of employment and 95% of family income (FAO, 2018). Sheep are kept in ASALS since in times of drought they can easily be de-stocked and re-stocked afterwards thus reducing production cost due to starvation (FAO, 2018).
Sheep grow at a faster rate, with high reproductive capacity and can withstand harsh environmental conditions, yet require minimum cost of production (Stephen, 2017). Therefore, there is need to increase sheep number and productivity through improved breeding, proper nutrition and management of production limiting diseases. Parasitic infections especially gastro-intestinal (GI) parasites are among the major production limiting diseases. Blood sucking nematode Haemonchus contortus and Eimeria species and Cryptosporidium species are the most important helminthes and coccidia respectively (McRae et al., 2015).
Production losses caused by these gastrointestinal parasites are manifested by mortality of up to 40%, reduction in milk, wool and live weight (up to 50 %). Besides, their higher susceptibility to GI parasites necessitates heavy reliance on anthelmintic therapy by farmers which has resulted to anthelmintic resistance (AR) (McRae et al., 2015).
Gastrointestinal parasites limits sheep productivity, farmers tend to rely on anthelmintic therapy resulting to occurrence of anthelmintic (Charlier et al., 2014). Hence the need to test for prevalence and intensity of these parasites, assess knowledge, practices and attitudes towards treatment and control of gastrointestinal parasites in sheep and test for anthelmintic resistance (AR) in selected sheep farms in Kasarani Nairobi County, Kenya.

 
1.1 OBJECTIVE
Investigation of the prevalence of helminthes and coccidial infestation, anthelmintic usage and anthelmintic resistance in selected sheep farms in Kasarani, Nairobi County.

1.2 SPECIFIC OBJECTIVES
1. To determine the prevalence, intensity and spectrum of helminthes and coccidial infestation in sheep
2. To assess knowledge, practice and attitude of farmers, veterinary service providers and agricultural and veterinary drugs sales persons towards control of helminthes and coccidia infestation in sheep.
3. To investigate the occurrence of anthelmintic resistance.

1.3 RESEARCH QUESTIONS
1. What is the prevalence of gastrointestinal parasites of sheep in the study area?

2. What are the farm level practices and farmer knowledge on use of anthelmintics in sheep flock?

3. Which anthelmintics has the parasites develop resistance to?

1.4 HYPOTHESIS
It is hypothesized that gastro-intestinal parasites infections in sheep limit their productivity hence inappropriate use of anthelmintics which result to anthelmintic resistance and presence of clinical and sub-clinical cases despite treatment.

1.5 JUSTIFICATION
Gastrointestinal parasitoses cause high mortalities, reduction in live weight and reduced overall sheep productivity. Determination of prevalence of gastrointestinal parasites is important in order to account for their impact in sheep production. Inadequate awareness of helminthes, their effects on sheep production, treatment and control is the knowledge gap that exists among sheep farmers in developing countries. Therefore, the need  to assess knowledge, practice and  attitude towards control and treatment of sheep’s helminthes. Anthelmintic resistance is a major challenge in the sheep production industry and it’s attributed to inappropriate anthelmintics usage hence the need for resistance testing. Sheep production is an importance social-economic activity for farmers in Kasarani sub-county. However adverse effects of gastrointestinal parasites limits sheep productivity which make farmers to rely on anthelmintic therapy which led to occurrence of anthelmintic resistance. Therefore, this study becomes relevant as it focuses on occurrence and levels of helminthes infection and resistance to anthelmintics and contributing factors.

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