The production of small ruminants is an attractive agricultural enterprise for Thai smallholder farmers because of lower inputs and high reproductive rate compared with cattle and buffalo, and their ability to thrive on native pasture that is unsuitable for crop production (Jittapalapong et al., 2012; Windsor et al., 2018). Sheep and goats are becoming increasingly important in Southeast Asia, particularly in regions with large Islamic populations such as Indonesia, Malaysia, and parts of the Philippines. (Windsor et al., 2018). Moreover, in recent years, demand for goat meat from Thailand and neighboring regions is increasing, particularly from Vietnam and Laos. This provides opportunities for smallholder farmers to increase productivity. In Thailand, goat production is traditionally extensive with low inputs, and subsequently low outputs. Five major small ruminant management systems have been described, including: tethering, free range, semi-free range, intensive, semi-rotational grazing and livestock-tree crop integrat
ed systems (Pralomkarn & Boonsanit, 2012). Free range is the most popular system typically practiced by small farmholders and consist of 10 – 60 animals per herd. It allows sheep and goats to browse alongside road verges, empty paddy fields, ample uncultivated areas and used public lands. In most systems, sheep and goats are herded back to the shelter in the evening and kept in small hutches overnight for protection.
An effective herd health program to maintain the health of livestock and prevent the occurrence of disease is necessary for rearing animals. Veterinary services are poor and knowledge about goat diseases is low or non-existent. An effective health management is only provided in commercial and governmental goat farms. Where investigations have occurred, these have mostly been performed by non-veterinarians, and animals being treated with antibiotics without regard to food safety and antimicrobial residue issues. Several investigations regarding health problems in goat have been conducted in Thailand for many years. Gastrointestinal parasite (GI) burdens are frequently associated with grazing management. Therefore, animals that graze communal pastures, are often at higher risk of exposure.
However, helminthic and protozoal infections have been reported among goats in Thailand (Worasing et al., 2011; Jittapalapong et al., 2012). It has also been found that GI parasitism among ruminants occurred all year round in tropical climates such as Thailand, with higher infection intensities during the rainy season (Jittapalapong et al., 2012). Temperature and humidity are primary factors involved in the development and survival of parasite eggs, larvae, cysts, and oocysts in the environment.
To date, the importance of caprine GI parasitic infections has not been investigated in detail in lower Northern Thailand. But, a comprehensive understanding of endoparasitism is crucial for the sustainable control of parasites that interact with hosts in a specific climate, management system and production environment. Improving goat production in Thailand requires prevalence studies to provide the evidence-basis for the practical approaches that can assist smallholder goat farmers to improve their husbandry and health practices for increasing goat productivity. The specific objectives of this investigation were to estimate the prevalence of GI parasitism of goats on smallholder farms reared under traditional production systems.
A cross-sectional study was conducted from May 2019 to January 2020 in Phitsanulok, lower northern Thailand. (16.78°North, 100.20°East). Five districts; Muaeng, Bangragarm, Phompiram, Wadbote and Bangkatum in Phitsanulok province were selected for this research (Fig. 1). These districts are located at an altitude of 44 m above sea level. These areas are characterised by a tropical continental climate by hot season (mid-February to mid-June), rainy season (mid-June to mid-October) and winter season (mid-October to mid-February), respectively. The average monthly temperature ranges from 18.7°C in January to 37.2°C in April and the monthly precipitation between 3.9 and 247.6 mm. It has mixed weather with a daily average relative humidity ranging from 62 to 81 % (Thai Meteorological Department, 2019). In total, goats from 31 smallholder farms were included.
In this research, goats were kept in the free-range environment. These animals grazed during the day and were housed overnight without feed supplements being provided. The selection of animals at the smallholder farms was dependent on the number and availability of animals per farmer, although not more than 8 samples were taken from the sampled herd, with gender and species considered. All goats in this study were crossbreds of Boer and Angro. Sampled animals were not treated with anthelmintics within the last 3 months.
The use of anthelmintics, particularly ivermectin (10 mg/30 kg bodyweight) and mebendazole (13 – 15 mg/kg bodyweight or 1 tablet of 500 mg/30 kg bodyweight), administered at doses widely considered as therapeutic in these species. The farmer administered anthelmintic treatments to his herd two to four times per year (rotating between ivermetin and mebendazole) with further treatments with levamisole (5 mg/kg bodyweight) for animals that were suspected to have severe parasitic infections (as determined by ocular examination for conjunctival pallor indicative of anaemia).
At each farm, at least 90 % of the individuals older than 3 months before the sample collection were sampled. A total of 885 goats raised on 31 different farms were taken. A sample size was determined within the expected prevalence of disease in the population of 0.01 and 95 % confidence and population size of >10,000 (Fosgate, 2009). Fecal samples were collected per-rectum using plastic gloves, put into fecal pots, labelled and kept cool before transportation to the laboratory and then stored at 4°C in the refrigerator until analysis to avoid hatching of the eggs. Body Condition Scoring. Body condition scores (BCS) were determined by physically feeling the level of muscling and fat deposition over and around the vertebrae in the loin region. This was categorised on a scale of 1 – 5, according to Friedricks (1993), where a score of 1 indicates thin and emacia- ted goats, while a score of 5 indicates obese goats.
The intensities of nematodes and coccidial infections were categorized by mean eggs per gram of feces (EPG) and oocysts per gram of feces (OPG), respectively. Fecal egg counts (FEC) and fecal oocyst counts (FOC) were done using a modified McMaster method (MAFF, 1986) with 60 ml of saturated NaCl solution as the flotation fluid (specific gravity = 1.2) and 4 g of feces to determine EPG and
All descriptive and analytical statistics were performed using the R-package. For the epidemiological studies, results of the FEC were used to calculate prevalence rates. The prevalence (p) of animals harbouring each parasite was calculated as p = d/n, where d is the number of animals diagnosed as having a given parasite at that point in time and n = number of animals at risk (examined) at that point in time (Thrusfield, 2005).
For purposes of analysis, animals with FEC values of gastro-intestinal nematode (GIN) were classified into GIN-free, low (<500 EPG), medium (500 – 1000 EPG) and high (>1000 EPG). Similarly, FOC values were classified into
Transforming non-normally distributed FEC and FOC data into a normal distribution was achieved using the log transformation
[log10(EPG+10) and log10(OPG+10)] prior to the analyses. Results for FEC and FOC were presented as arithmetic means ± standard deviation.
The association between independent factors (sex) and continuous dependent variables (EPG, OPG and trematode intensity) was calculated using one way analysis of variance (ANOVA). The association between the independent factors and the prevalence of the χ various parasites were evaluated using Chi-square statistic. The correlations between the occurrences (and intensity) of the parasites was undertaken using the Pearson partial correlation (rho, r). The difference in parasite loads for host sex and body condition score were tested by ANOVA. Moreover, correlations between variables were determined by Pearson’s correlation. In all the analysis, confidence level was held at 95 %, and
Аpprovals for using animals in the current study were obtained from the ethical/IACUC committee at the Naresuan University, Phitsanulok, Thailand (Permit Number: NU-AG620504). The research has been complied with all the relevant national regulations and institutional policies for the care and use of animals.
Descriptive statistics (number and percentage of positive samples and mean, SD, Min, and Max) of fecal egg/oocyte counts in goats of 31 Smallholder Farms in Thailand.
Variables | Examined | Positive [ |
Mean | SD | Min – Max |
---|---|---|---|---|---|
Gastrointestinal strongyles | 885 | 680 (76.8%) | 799.0 | 1348.6 | 0 – 13333 |
885 | 4 (0.5%) | 0.2 | 3.4 | 0.58 | |
885 | 8 (0.9%) | 0.6 | 7.1 | 0 – 104 | |
885 | 1 (0.1%) | 1.5 | 1.5 | 0 – 1368 | |
885 | 445 (50.3%) | 427.6 | 118.1 | 0 – 96285 | |
885 | 132 (14.2%) | 69.5 | 20.0 | 0 – 15786 | |
Others ( |
885 | 6 (0.7%) | 0.6 | 0.3 | 0 – 246 |
Third-stage larvae identified in coprocultures were dominated by
Third-stage strongylid larvae identified in coprocultures of goats (expressed as mean percentage).
Larval genus | Total (%) |
---|---|
55.84 | |
20.53 | |
5.80 | |
5.00 | |
4.18 | |
3.46 | |
3.07 | |
0.92 | |
0.85 |
The total prevalence did not vary between sexes (
Prevalence of helminth infections (percentage of infected goats) in male and female goats in Northern Thailand.
Parasitic infection | Male |
Female |
X2 | |||||
---|---|---|---|---|---|---|---|---|
Total | + | % | Total | + | % | |||
Strongyles | 29 | 24 | 82.8 | 856 | 656 | 76.6 | 0.591 | 0.442 |
29 | 0 | 0 | 856 | 4 | 0.5 | 0.136 | 0.712 | |
29 | 0 | 0 | 856 | 8 | 0.9 | 0.274 | 0.601 | |
29 | 0 | 0 | 856 | 1 | 0.1 | 0.034 | 0.854 | |
29 | 15 | 51.7 | 856 | 430 | 50.2 | 0.025 | 0.875 | |
29 | 3 | 10.3 | 856 | 129 | 15.1 | 0.494 | 0.482 | |
Others ( |
29 | 0 | 0 | 856 | 6 | 0.7 | 0.205 | 0.651 |
Total: total number of examined animals; +: number of infected animals.
Male goats had higher prevalence (
There were no significant associations between the presence of parasites and sex (male vs female), although body condition showed significant difference (P = 0.009) on the prevalence of
Contingency table and odds ratio results for association of explanatory variables with parasites positive for fecal eggs of goats, by parasites.
Variables | Infected/ Examined | Prevalence (%) | 95% CI | Odds Ratio | |
---|---|---|---|---|---|
Stronglyes (%) | |||||
Sex | 0.402 | ||||
Female | 656/856 | 76.6 | 74.8 – 88.2 | 1.0 | |
Male | 24/29 | 82.8 | 46.7 – 91.3 | 0.654 | |
Body Condition Score | 0.163 | ||||
Good | 23/30 | 76.7 | 43.2 – 87.6 | 1.0 | |
Moderate | 613/805 | 76.1 | 73.5 – 90.3 | 0.426 | |
Poor | 44/50 | 88.0 | 76.3 – 99.7 | 0.430 | |
Sex | 0.511 | ||||
Female | 129/856 | 15.1 | 10.4 – 21.8 | 1.0 | |
Male | 3/29 | 2.3 | 1.3 – 24.9 | 0.650 | |
Body Condition Score | 0.828 | ||||
Good | 4/30 | 13.3 | 11.1 – 26.5 | 1.0 | |
Moderate | 119/805 | 14.8 | 6.3 – 20.6 | 0.735 | |
Poor | 9/50 | 18.0 | 8.1 – 27.9 | 0.799 | |
Sex | 0.895 | ||||
Female | 430/856 | 50.2 | 50.2 – 66.2 | 1.0 | |
Male | 15/29 | 51.7 | 14.2 – 66.8 | 0.895 | |
Body Condition Score | 0.009 | ||||
good | 15/30 | 50.0b | 13.2 – 65.7 | 1.0 | |
Moderate | 394/805 | 48.9b | 42.4 – 62.3 | 0.383 | |
Thin | 36/50 | 72.0a | 58.2 – 85.8 | 0.372 |
Values with different letters within a column in each variable differ significantly (
Results from a predictive logistic regression model for parasitic infection in goats from Northern Thailand.
Variable | Level | β | SE | Wald | OR | P-Value | 95% CI |
---|---|---|---|---|---|---|---|
Sex | Male | 1 | - | - | |||
Female | -0.16 | 0.502 | 0.102 | 0.852 | 0.750 | 0.319 – 2.278 | |
Body Condition Score | Good | 1 | - | - | |||
Moderate | -0.853 | 0.718 | 1.412 | 0.426 | 0.235 | 0.104 – 1.740 | |
Thin | -1.061 | 0.529 | 4.023 | 0.346 | 0.045 | 0.123 – 0.976 |
β: regression coefficient; SE: standard error; OR: odds ratio; CI: 95% confidence interval; *: denotes significance (
The mean burden of different helminthes was assessed according to sex, and body condition. The infection level of GIN based on FEC was various and ranged from 0 to 15,786 with a mean value of 802.1 (± 45.5) EPG. Eleven samples had more than 5,000 eggs. As presented in Table 6, 17.2 % of males and 22.8 % of females were GIN-negative. In both sexes, the proportion of samples classified as low (<500 EPG) ranged between 38 – 52 %. While 13.8 % of males and 25.4 % of females were classified as high (>1000 EPG), respectively. In females, 47 % of the samples were classified as low (<1800 OPG) and 2.7 % as medium (1800 – 6000 OPG). Around 48 % of the samples collected from males were
Results of the fecal egg (expressed as eggs per gram, EPG) and oocyst (expressed as oocysts per gram, OPG) counts differentiated for the prevalence of gastrointestinal strongylid nematodes (GIN) (classified as negative, low, moderate and high), separated by sex and species ( expressed as % within sex or body condition score).
Sex |
Body condition score |
Total | ||||
---|---|---|---|---|---|---|
Male | Female | Poor | Moderate | Good | ||
Gastrointestinal strongylid | nematodes | (GIN) | ||||
Mean FECc | 455.5 ± 132.8b | 810.7 ± 46.6a | 1603.3 ± 287.2A | 751.3 ± 45.4B | 738.5 ± 202.78B | 802.1 ± 45.4 |
Negative | 17.2 | 22.8 | 12.0 | 23.2 | 23.3 | 22.6 |
Low (< 500 EPG) | 51.7 | 38.3 | 38.0 | 38.8 | 40.0 | 38.8 |
Moderate (500 – 1000 EPG) | 17.2 | 13.6 | 6.0 | 14.0 | 16.7 | 13.7 |
High (> 1000 EPG) | 13.8 | 25.4 | 44.0 | 24.0 | 20.0 | 25.0 |
Mean FOCc | 591.1 ± 245.1 | 422.0 ± 121.8 | 172.8 ± 118.1 | 412.8 ± 124.9 | 1248.9 ± 945.8 | 427.6 ± 118.1 |
Negative | 48.3 | 49.5 | 28.0 | 50.8 | 50.0 | 49.5 |
Low (< 1800 OPG) | 37.9 | 47.0 | 72.0 | 45.2 | 43.3 | 46.7 |
Moderate (1800 – 6000 OPG) | 13.8 | 2.7 | 0 | 3.2 | 3.3 | 3.1 |
High (> 6000 OPG) | 0 | 0.8 | 0 | 0.7 | 3.3 | 0.8 |
Mean ± standard error of the mean (SEM)
A,Bdifferent uppercase superscripts indicate statistical difference of FEC or FOC between body condition score at
a,bdifferent uppercase superscripts indicate statistical difference of FEC or FOC between sex at
The present study shows high prevalence of helminths and
The current findings revealed that the animals were affected by a wide variety of parasites. The findings are useful in identifying areas for improvement and modification of current helminth control strategies, so as to minimize the impact of GI parasites on productivity. The overall GI parasites prevalence of 87.2 % observed in the present study is, however, higher than the prevalence of GI parasites in goats in Laos (73 %) (Windsor et al., 2018), Bangladesh (74.8 %) (Islam et al., 2017) and another study from Thailand (79 %) (Jittapalapong et al., 2012). This difference may be attributed to different sampling sites, seasons, animal breeds, management and agro-climatic conditions. The data, however, is a useful confirmation of concerns that there is a need to control GI parasites in this region.
The types of parasites found in this study included gastrointestinal nematodes, cestodes, trematodes and protozoa. Our observations were similar to those of some other studies conducted in Asia and abroad, which described strongyle infection as a major problem in small ruminants (Zvinorova et al., 2016; Lambertz et al., 2018; Windsor et al., 2018; Sharma, 2020). The proportions of the nematode genera according to L3 larvae in the current study in which
The most prevalent nematodes were Strongyles, with
Infection by trematodes had the lowest prevalence (0.1 %) among examined animals. This finding was closely related to reported in southern Thailand that 0.79 % of goats were infected by
On the other hand, the only cestodes identified through fecal examination in this study were
The prevalence of
The results of sex-related prevalence of GI parasites revealed that GI parasites infection occurred with similar frequency in males and females, which can be attributed to the fact that both sexes are kept under similar management systems (Windsor et al., 2018; Mpofu et al., 2020). On the contrary, the significant association between host sex and the prevalence of GI parasites was previously reported to occur more often in females higher than male (Islam et al., 2017; Singh et al., 2017). It is interesting to note that females are assumed to be more heavily infected due to stress and low immune status during pregnancy, parturient paresis and lactation periods (Golo et al., 2017).
In this study, the coproculture also showed that the predominant worm species were
This study was consistent with the findings of Biswas et al. (2014) and Admasu & Nurlign (2014), who discovered higher parasite infection in poor body condition animals compared to moderate and good condition hosts. Indeed, malnutrition and other concurrent parasitic infection will result in a weak immune response in the host to the parasites’ infective stage (Watson et al., 1994). Meanwhile, Etter et al. (1999) discovered increasing parasite fecundity in immunocompromised animals. Infection of small ruminants with coccidia and strongyles leads to gastroenteritis, protein-losing enteropathy, poor weight gain, and loss of body condition (Soulsby, 1982; Idika et al., 2012).
In conclusion, based on findings from this study, natural infections with gastrointestinal parasites in goats in Phitsanulok are common. The infection level of GIN based on FEC was moderate to high and involved infections with multi-species.