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Epidemiology and seasonal dynamics of adult Haemonchus contortus in goats of Aligarh, Uttar Pradesh, India.
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Epidemiology and seasonal dynamics of adult Haemonchus contortus in goats of Aligarh, Uttar Pradesh, India. ⁎
Sadia Rashid , Malik Irshadullah Section of Parasitology, Department of Zoology, Aligarh Muslim University, Aligarh-202002, India
A R T I C L E I N F O
A B S T R A C T
Keywords: Epidemiology Haemonchus contortus Prevalence Infection indices Seasonal dynamics
A survey was carried out to determine the prevalence and seasonal abundance of Haemonchus contortus in the semi arid zone of Uttar Pradesh, India between January 2010 to December 2013. Entire gastrointestinal tract from slaughtered goats were brought to the laboratory. Parasites were collected from the abomasum, counted and recorded on monthly basis. The collected data were analyzed on the basis of temperature, rainfall and humidity of the months/seasons. Out of total 635 goats, 383 (60%) were found to be infected with H. contortus. The mean intensity and abundance was found as 354 and 263 respectively. Marked variations in the prevalence, mean intensity and abundance were noticed during different month/season of the year. Highest values of these infection indices were found in the rainy season and lowest in summer. Although prevalence, intensity and abundance were positively correlated with temperature, rainfall and humidity but only the effect of rainfall was found to be statistically significant. The present study provides a consolidated account on the seasonal dynamics of H. contortus, which can be used for integrated control measures of this blood sucking parasite under local environment conditions.
1. Introduction
Irshadullah, 2014). The usual mode of control of haemonchosis is based on the repeated use of anthelmintics. However, indiscriminate uses of anthelmintics in organized and private farms cause multiple drug resistant among parasites, which is currently a major issue in the production of small ruminants in different parts of India. Because of development of drug resistance among gastrointestinal nematodes alternative control strategies like rotational grazing, selective breeding, nutritional supplementation, selective treatment and use of plants, containing natural anthelminthics are being used to cope with increasing anthelmintics resistance (Sahoo and Khan, 2016). Efficient and effective parasite control is only possible if sufficient information is available on prevailing epidemiological factors which determine the frequency and transmission of diseases (Barger 1999). Many studies around the world have confirmed that the development and survival of H. contortus depends upon various climatic factors (Fernández et al., 1994; Miro et al., 1991; Connor et al., 2007, 2006;). This situation warns the need of comprehensive epidemiological knowledge in order to devise an appropriate and cost effective strategy to control this parasite. Literature survey reveals that H. contortus is one of the most dominating parasites of sheep and goats and is quite prevalent throughout the world (Akkari et al., 2013; Asif et al., 2008; Burke et al., 2016; Gebresilassie and Tadele, 2015; Holm et al., 2014; Miller et al., 1998;
India is basically an agricultural country where almost 70% of the population depends on agriculture for livelihood (Delphine and Thatheyus, 2003). Rearing of livestock is an integral part of agriculture where over 15–20% families are landless and about 80% of the land holders belong to the category of small and marginal farmers (Anon, 2010). The rural livestock population is still reared on grazing based system and breeding is mostly done through the natural method although artificial insemination is now practiced by the government institutes to improve the productivity (Anon, 2017). Parasitic infections are highly prevalent in India due to its hot and humid climate, which favours the development and survival of parasites. Among the diseases that constrain the survival and productivity of sheep and goats, gastrointestinal nematode infection ranks highest on a global index on the basis of their impact on poor with Haemonchus contortus being of overwhelming importance (Perry et al., 2002). H.contortus is a haematophagous parasite of small ruminants and a significant cause of morbidities and mortalities worldwide especially in warm and moist climate. The importance of this worm is due to combination of high fecundity and a short developmental period that provides an enviable developmental plasticity for adaptation/resistance to control measures (Besier et al., 2016; Emery et al., 2016; Rashid and
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Corresponding author. E-mail addresses: [email protected] (S. Rashid), [email protected] (M. Irshadullah).
https://doi.org/10.1016/j.smallrumres.2018.01.018 Received 3 November 2016; Received in revised form 26 January 2018; Accepted 28 January 2018 0921-4488/ © 2018 Elsevier B.V. All rights reserved.
Please cite this article as: Rashid, S., Small Ruminant Research (2018), https://doi.org/10.1016/j.smallrumres.2018.01.018
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2.3. Sample collection and examination
Nahar et al., 2015; Rajapakseet al., 2008; Tan et al., 2014; Uriarte et al., 2003; Vlassoff et al., 2001) as well as in many parts of India (Bandyopadhyay et al., 2010; Bukhari and Sanyal, 2011; Mir et al., 2013; Palanivel et al., 2012; Pathak and Pal, 2008; Shirale and Made, 2007; Singh et al., 2015,1997; Sood, 1983; Sutar et al., 2010; Tariq et al., 2010) but no comprehensive studies have been done so far in Aligarh district of Uttar Pradesh. Therefore in the present study the seasonal dynamics and the effect of various environmental factors on the prevalence of H. contortus in goats was studied in Aligarh district, a semi-arid region of north India.
The entire gastrointestinal tracts were collected twice a week from goats of approximately an year old, slaughtered at the Aligarh abattoir and brought to the laboratory in separate plastic bags. Abomasum was separated from GI tract, opened longitudinally and the content was collected in a large beaker. The mucosae were washed with Hanks balanced salt solution (HBSS) and washing was drained in the same beaker and then carefully scraped to remove any adhering worms. If the worms were embedded in the mucosa they were removed with the help of forceps. The entire washings from the abomasum were diluted with HBSS and examined for worms. H. contortus worms were separated, counted and recorded on monthly basis. The obtained data on H. contortus were used to calculate the prevalence, mean intensity and abundance (infection indices) according to the following formulae as given by Margolis et al. (1982).
2. Materials and methods 2.1. Study area The present study was carried out from January 2010 to December 2013 in Aligarh district, located in the western part of Uttar Pradesh approximately 140 km south-east of the capital city, New Delhi. It lies between 27°53′N, 78°05′E and 27°88′N, 78°08′E coordinates, covering a total area of 3747 square km and having a population of about 3.7 million. It has an elevation of approximately 178 m. The city is in the middle portion of the doab, the land between the Ganga and the Yamuna rivers (Anon, 2011a,b). The total livestock population in Aligarh district is about 1.05 million, among which there are 153,453 cattle, 841,392 buffaloes, 11,841 sheeps, 172,196 goats and 25,711 pigs (Anon, 2013).
Prevalence(%) Total number of individuals infected with particular parasite species : Total number of host examined × 100
Mean intensity:
Total number of individuals of a particular parasite species Total number of infected individuals of the species
Abundance Total number of individuals of a particular parasite species : Total number of the host species examined (infected+uninfected) Furthermore, the data were analyzed on the basis of temperature, rainfall and relative humidity of different months of the year, to assess the influences of meteorological factors.
2.2. Climate Aligarh has a monsoon-influenced climate typically that of subtropical humid type with three types of seasons, summer (March to June), rainy/monsoon (July to September) and winter (October to February) (O’Hare, 1997). Mean temperature, relative humidity and rainfall during different months/season is presented in Table 1, which is based on the data collected from the Meteorological Centre, Department of Physics, Aligarh Muslim University, Aligarh. Summer is very hot in Aligarh, with maximum temperature (46 °C) recorded in May. The average temperature range in summer is about 25–35 °C. The rainy season starts from late June and continues till September. Annual rainfall in Aligarh district was recorded as 899 mm out of which about 80% was received during the monsoon period. Winters are usually very cold in December and January where temperature drops to ˂2 °C. The relative humidity was comparatively low during summer and high during rainy and winter seasons.
2.4. Statistical analysis Pearson’s correlation coefficient was calculated by using SPSS 16 (SPSS Inc., USA) to assess the association between meteorological factors and infection indices throughout the year. Chi Square analysis was used to find out the significant differences between prevalence values of different months of the year whereas Kruskal–Wallis test (nonparametric ANOVA) was performed to determine the significant differences between the values of mean intensity and abundance during different months. p value ≤ 0.05 was considered as significant. The software used was Graph Pad Instat version 3.06, (Graph Pad Software, U.S.A). 3. Result A total of 635 abomasa were examined among which 383 (60%) were found to be infected with H. contortus. The mean intensity and abundance was found as 354 and 263 respectively. Although, goats were found to be infected with H. contortus throughout the year but considerable variations were noticed in the worm burden during different months. The prevalence was highest in the month of August (96.66%) followed by September (90.38%) while the lowest infection was recorded in January (24.48%) and February (31.81%) (Table 2). Statistical analysis by Chi square test revealed significant difference between the prevalence rate of all months (χ = 79.85, p < 0.001). It was observed that prevalence rate declines with the decrease of temperature from 29 °C (August) to 10 °C (January) and then slowly increases with the rise of temperature. Low prevalence was found in those months in which either temperature is very high (June, 34 °C) or very low (January, 12.8 °C). Prevalence of H. contortus was found higher during monsoon season (July–September) and then decreases with the decline of rainfall. Relative humidity was found to be partially related with the prevalence. It was noticed that when the relative humidity was below 40% (April and May) the prevalence rate was low, whereas in August when the humidity was very high (85%) the prevalence rate was
Table 1 Mean temperature, relative humidity and rainfall during different months of the year in Aligarh city (2010–2013). Source: Metrological Center, Department of Physics, A.M.U., Aligarh. Month
Temperature (°C)
Rainfall (mm)
Relative humidity (%)
January February March April May June July August September October November December
12.8 17.7 24.5 29.8 33.7 34.7 30.1 29.3 28.7 26.4 21.1 15.6
10 (0.1–16.2) 30 (1.6–27) 1 (0.4–1.8) 11 (0.1–12.6) 20 (0.1–26.2) 73 (0.4–94.6) 285 (1–103.6) 249 (0.2–69.2) 198 (0.1–122.6) 11 (1.6–7.4) 5 (0.2–11) 6 (0.6–12.8)
71 74 57 39 39 54 79 85 75 65 69 76
(1.4–26.5) (7.4–31.5) (10–38.5) (18.2–43.8) (21–46.4) (27–44.6) (25–38.6) (25–35) (23.4–36) (16–35) (10–32) (4–24)
(49–98) (36–98) (27–90) (15–78) (17–66) (22–98) (46–98) (63–100) (61–98) (38–98) (42–94) (48–97)
Values are the mean of 4 years data (2010–2013). Values in parenthesis represent the minimum and maximum range.
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rate and severity of H. contortus infection (Getachew et al., 2007). The prevalence of H. contortus showed a definite seasonal trend that corresponds with the rainfall pattern in the study area. Maximum prevalence, mean intensity and abundance were recorded during rainy season while minimum during summer season which may be due to more availability of infective larvae (L3) on the pasture from where the animals acquire infection. Similar results have also been reported from Rajasthan (Singh et al., 1997), Maharashtra (Shirale and Made, 2007; Sutar et al., 2010), Assam (Bulbul et al., 2015; Hafiz et al., 2016), and Tamil Nadu (Varadharajan and Vijayalakshmi, 2015). These authors (loc.cit) suggested that environmental conditions during the rainy season are conducive for the development of infective larvae and high rainfall helps in larval dispersion on the herbage, which increases the chance of contact between host and parasite. Probably moderate temperature and high humidity during monsoon period may be more suitable for the development and survivals of infective stage of H. contortus. Rainfall may also help in the dispersion of larvae on pasture and thereby increases the chances of host’s contact with infective larvae (Katoch, 1998; Santos et al., 2012; Sanyal 1989a). Soulsby (1966) suggested that high rainfall during monsoon season provides suitable molarity of salts in the soil which enhance ecdysis and thereby transformation of L1 to L3 takes place easily. It is an established fact that the maximum growth of herbage occurs during rainy season, which may favour the survival and migration of larvae. Sanyal (1989b) studied the bionomics of pre-parasitic stages of ovine strongyle in faeces and on pasture and found that when there was sufficient rainfall, larvae were found to migrate vertically up to 15 cm and laterally up to 50 cm as compared to only 5 cm and 20 cm, respectively during non-rainy season. He further stated that infective larvae survive on pasture for more than 11 weeks in rainy season. Agyei and Amponsah (2001) and Silva et al. (2008) reported significant positive relationship between the level of infective larvae on herbage and rainfall. Higher temperature and rainfall cause stress to the host which lowers its immunity and predisposes it to a heavy infection (Hawkins, 1945). Low prevalence rate during summer and winter could be explained by the fact that these seasons are not conducive for the development of the infective larvae and therefore contamination of pasture were low. O’Connor et al. (2006) reported highest level of pasture contamination with free-living infective larvae (L3) during rainy while, lowest during dry season. The grass cover on the grazing pasture during dry season is reduced by which the eggs/larvae are exposed to desiccation, which either causes high mortality of larvae or they migrate deep into the soil (Ng’ang’a et al., 2004; Vlassoff, 1982). Urquhart et al. (1996) reported that the development of eggs become slow at low temperature and below 10 °C the development of L3 from eggs is stopped. It can be suggested from the present findings that 25–30 °C temperature, 75–85% relative humidity and more than 50 mm rainfall is more suitable for the development of infective stages of H. contortus. Similarly, Nahar et al. (2015) reported 29.8 °C temperature, 146 mm rainfall and 86% relative humidity are more suitable for larval development. O’Connor et al. (2006) reported that the development of eggs to infective larvae of H. contortus occur at 23–36 °C temperature and 70% relative humidity.
Table 2 Prevalence, mean intensity and abundance of Haemonchus contortus during different months of the year. Month
Number of animals examined
Number of infected animals
Prevalence (%)
Mean Intensity
Abundance
January February March April May June July August September October November December Total
49 44 49 50 58 58 51 60 52 50 53 61 635
12 14 18 20 32 26 38 58 47 43 38 37 383
24.48 31.81 36.73 40.00 55.17 44.82 74.50 96.66 90.38 86.00 71.69 60.65 60.31
75 88 93 128 324 264 526 786 640 588 438 306 354
18 28 34 51 178 118 391 759 578 505 314 185 263
Values are the mean of 4 years data (2010–2013).
found maximum. Although humidity was high (71–74%) in the month of January and February, prevalence was found very low which indicates that other factors like temperature and rainfall play a role in the prevalence. Variation in the mean intensity and abundance were also observed during different months. Highest values of these were found in August followed by September, while lowest values were recorded in January, February and March (Table 2). Mean intensity and abundance was found higher in those months which has moderate temperature (29 °C), high rainfall and maximum relative humidity. However, the values of both of these infection indices decline in those months which had extreme temperature either very low (13° C) or very high (35° C). Mean intensity and abundance showed a declining trend following the start of the dry spell from November. Statistical analysis of monthly data obtained for mean intensity and abundance by Kruskal-Wallis test, shows a highly significant difference in the mean intensity (KW = 45.24, p < 0.001) and abundance (KW = 46.13, p < 0.001). Analysis of Pearson’s correlation coefficient revealed that prevalence, intensity and abundance were positively correlated with the temperature, rainfall and relative humidity (Table 3). However prevalence, mean intensity and abundance were strongly related (r ≥ 0.6) with rainfall (p ≤ 0.05) and weakly related with temperature and humidity (r ≤ 0.1 − 0.5). 4. Discussion About 60% goats were found to be infected with H. contortus in Aligarh region. Similar results have also been reported from Kashmir valley (Tariq et al., 2008), Jammu region (Khajuria et al., 2013) and Meghalaya (Bandyopadhyay et al., 2010). Contrary to our findings either very high (70- 96%) or very low (6–36%) prevalence of H. contortus have been reported from many parts of India (Pathak and Pal, 2008; Sharma et al., 2009; Prakash and Bano, 2009; Mir et al., 2013). Such variation in the prevalence rate may be due to differences in the sample size, prevailing agro-climatic conditions, nutritional status and availability of susceptible hosts. As it has been reported that age, breed, nutrition and physiological state of the host influences the incidence
5. Conclusion H. contortus infections in goats at Aligarh, North India, showed a
Table 3 Prevalence, mean intensity and abundance of Haemonchus contortus during different seasons of the year. Seasons
Months
Number of animals examined
Number of infected animals
Prevalence (%)
Mean Intensity
Abundance
Summer Rainy Winter
Mar–Jun July–Sept Oct–Feb
215 163 257
96 143 144
44.18 87.18 54.92
202 650 299
95.25 576 210
Values are the mean of 4 years data (2010–2013).
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well-defined seasonal pattern. Rainfall seems to be the major limiting factor on the prevalence and worm burden as compared to temperature and humidity. The present findings may be used as a baseline data for developing an epidemiologically based control strategies for H. contortus in this region and may be helpful to stop indiscriminate use of anthelmintics. In the present study the effect of climatic factors on the survival of eggs/larvae was not studied, therefore, further studies are required.
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Short communication
Epidemiology and seasonal dynamics of adult Haemonchus contortus in goats of Aligarh, Uttar Pradesh, India. ⁎
Sadia Rashid , Malik Irshadullah Section of Parasitology, Department of Zoology, Aligarh Muslim University, Aligarh-202002, India
A R T I C L E I N F O
A B S T R A C T
Keywords: Epidemiology Haemonchus contortus Prevalence Infection indices Seasonal dynamics
A survey was carried out to determine the prevalence and seasonal abundance of Haemonchus contortus in the semi arid zone of Uttar Pradesh, India between January 2010 to December 2013. Entire gastrointestinal tract from slaughtered goats were brought to the laboratory. Parasites were collected from the abomasum, counted and recorded on monthly basis. The collected data were analyzed on the basis of temperature, rainfall and humidity of the months/seasons. Out of total 635 goats, 383 (60%) were found to be infected with H. contortus. The mean intensity and abundance was found as 354 and 263 respectively. Marked variations in the prevalence, mean intensity and abundance were noticed during different month/season of the year. Highest values of these infection indices were found in the rainy season and lowest in summer. Although prevalence, intensity and abundance were positively correlated with temperature, rainfall and humidity but only the effect of rainfall was found to be statistically significant. The present study provides a consolidated account on the seasonal dynamics of H. contortus, which can be used for integrated control measures of this blood sucking parasite under local environment conditions.
1. Introduction
Irshadullah, 2014). The usual mode of control of haemonchosis is based on the repeated use of anthelmintics. However, indiscriminate uses of anthelmintics in organized and private farms cause multiple drug resistant among parasites, which is currently a major issue in the production of small ruminants in different parts of India. Because of development of drug resistance among gastrointestinal nematodes alternative control strategies like rotational grazing, selective breeding, nutritional supplementation, selective treatment and use of plants, containing natural anthelminthics are being used to cope with increasing anthelmintics resistance (Sahoo and Khan, 2016). Efficient and effective parasite control is only possible if sufficient information is available on prevailing epidemiological factors which determine the frequency and transmission of diseases (Barger 1999). Many studies around the world have confirmed that the development and survival of H. contortus depends upon various climatic factors (Fernández et al., 1994; Miro et al., 1991; Connor et al., 2007, 2006;). This situation warns the need of comprehensive epidemiological knowledge in order to devise an appropriate and cost effective strategy to control this parasite. Literature survey reveals that H. contortus is one of the most dominating parasites of sheep and goats and is quite prevalent throughout the world (Akkari et al., 2013; Asif et al., 2008; Burke et al., 2016; Gebresilassie and Tadele, 2015; Holm et al., 2014; Miller et al., 1998;
India is basically an agricultural country where almost 70% of the population depends on agriculture for livelihood (Delphine and Thatheyus, 2003). Rearing of livestock is an integral part of agriculture where over 15–20% families are landless and about 80% of the land holders belong to the category of small and marginal farmers (Anon, 2010). The rural livestock population is still reared on grazing based system and breeding is mostly done through the natural method although artificial insemination is now practiced by the government institutes to improve the productivity (Anon, 2017). Parasitic infections are highly prevalent in India due to its hot and humid climate, which favours the development and survival of parasites. Among the diseases that constrain the survival and productivity of sheep and goats, gastrointestinal nematode infection ranks highest on a global index on the basis of their impact on poor with Haemonchus contortus being of overwhelming importance (Perry et al., 2002). H.contortus is a haematophagous parasite of small ruminants and a significant cause of morbidities and mortalities worldwide especially in warm and moist climate. The importance of this worm is due to combination of high fecundity and a short developmental period that provides an enviable developmental plasticity for adaptation/resistance to control measures (Besier et al., 2016; Emery et al., 2016; Rashid and
⁎
Corresponding author. E-mail addresses: [email protected] (S. Rashid), [email protected] (M. Irshadullah).
https://doi.org/10.1016/j.smallrumres.2018.01.018 Received 3 November 2016; Received in revised form 26 January 2018; Accepted 28 January 2018 0921-4488/ © 2018 Elsevier B.V. All rights reserved.
Please cite this article as: Rashid, S., Small Ruminant Research (2018), https://doi.org/10.1016/j.smallrumres.2018.01.018
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2.3. Sample collection and examination
Nahar et al., 2015; Rajapakseet al., 2008; Tan et al., 2014; Uriarte et al., 2003; Vlassoff et al., 2001) as well as in many parts of India (Bandyopadhyay et al., 2010; Bukhari and Sanyal, 2011; Mir et al., 2013; Palanivel et al., 2012; Pathak and Pal, 2008; Shirale and Made, 2007; Singh et al., 2015,1997; Sood, 1983; Sutar et al., 2010; Tariq et al., 2010) but no comprehensive studies have been done so far in Aligarh district of Uttar Pradesh. Therefore in the present study the seasonal dynamics and the effect of various environmental factors on the prevalence of H. contortus in goats was studied in Aligarh district, a semi-arid region of north India.
The entire gastrointestinal tracts were collected twice a week from goats of approximately an year old, slaughtered at the Aligarh abattoir and brought to the laboratory in separate plastic bags. Abomasum was separated from GI tract, opened longitudinally and the content was collected in a large beaker. The mucosae were washed with Hanks balanced salt solution (HBSS) and washing was drained in the same beaker and then carefully scraped to remove any adhering worms. If the worms were embedded in the mucosa they were removed with the help of forceps. The entire washings from the abomasum were diluted with HBSS and examined for worms. H. contortus worms were separated, counted and recorded on monthly basis. The obtained data on H. contortus were used to calculate the prevalence, mean intensity and abundance (infection indices) according to the following formulae as given by Margolis et al. (1982).
2. Materials and methods 2.1. Study area The present study was carried out from January 2010 to December 2013 in Aligarh district, located in the western part of Uttar Pradesh approximately 140 km south-east of the capital city, New Delhi. It lies between 27°53′N, 78°05′E and 27°88′N, 78°08′E coordinates, covering a total area of 3747 square km and having a population of about 3.7 million. It has an elevation of approximately 178 m. The city is in the middle portion of the doab, the land between the Ganga and the Yamuna rivers (Anon, 2011a,b). The total livestock population in Aligarh district is about 1.05 million, among which there are 153,453 cattle, 841,392 buffaloes, 11,841 sheeps, 172,196 goats and 25,711 pigs (Anon, 2013).
Prevalence(%) Total number of individuals infected with particular parasite species : Total number of host examined × 100
Mean intensity:
Total number of individuals of a particular parasite species Total number of infected individuals of the species
Abundance Total number of individuals of a particular parasite species : Total number of the host species examined (infected+uninfected) Furthermore, the data were analyzed on the basis of temperature, rainfall and relative humidity of different months of the year, to assess the influences of meteorological factors.
2.2. Climate Aligarh has a monsoon-influenced climate typically that of subtropical humid type with three types of seasons, summer (March to June), rainy/monsoon (July to September) and winter (October to February) (O’Hare, 1997). Mean temperature, relative humidity and rainfall during different months/season is presented in Table 1, which is based on the data collected from the Meteorological Centre, Department of Physics, Aligarh Muslim University, Aligarh. Summer is very hot in Aligarh, with maximum temperature (46 °C) recorded in May. The average temperature range in summer is about 25–35 °C. The rainy season starts from late June and continues till September. Annual rainfall in Aligarh district was recorded as 899 mm out of which about 80% was received during the monsoon period. Winters are usually very cold in December and January where temperature drops to ˂2 °C. The relative humidity was comparatively low during summer and high during rainy and winter seasons.
2.4. Statistical analysis Pearson’s correlation coefficient was calculated by using SPSS 16 (SPSS Inc., USA) to assess the association between meteorological factors and infection indices throughout the year. Chi Square analysis was used to find out the significant differences between prevalence values of different months of the year whereas Kruskal–Wallis test (nonparametric ANOVA) was performed to determine the significant differences between the values of mean intensity and abundance during different months. p value ≤ 0.05 was considered as significant. The software used was Graph Pad Instat version 3.06, (Graph Pad Software, U.S.A). 3. Result A total of 635 abomasa were examined among which 383 (60%) were found to be infected with H. contortus. The mean intensity and abundance was found as 354 and 263 respectively. Although, goats were found to be infected with H. contortus throughout the year but considerable variations were noticed in the worm burden during different months. The prevalence was highest in the month of August (96.66%) followed by September (90.38%) while the lowest infection was recorded in January (24.48%) and February (31.81%) (Table 2). Statistical analysis by Chi square test revealed significant difference between the prevalence rate of all months (χ = 79.85, p < 0.001). It was observed that prevalence rate declines with the decrease of temperature from 29 °C (August) to 10 °C (January) and then slowly increases with the rise of temperature. Low prevalence was found in those months in which either temperature is very high (June, 34 °C) or very low (January, 12.8 °C). Prevalence of H. contortus was found higher during monsoon season (July–September) and then decreases with the decline of rainfall. Relative humidity was found to be partially related with the prevalence. It was noticed that when the relative humidity was below 40% (April and May) the prevalence rate was low, whereas in August when the humidity was very high (85%) the prevalence rate was
Table 1 Mean temperature, relative humidity and rainfall during different months of the year in Aligarh city (2010–2013). Source: Metrological Center, Department of Physics, A.M.U., Aligarh. Month
Temperature (°C)
Rainfall (mm)
Relative humidity (%)
January February March April May June July August September October November December
12.8 17.7 24.5 29.8 33.7 34.7 30.1 29.3 28.7 26.4 21.1 15.6
10 (0.1–16.2) 30 (1.6–27) 1 (0.4–1.8) 11 (0.1–12.6) 20 (0.1–26.2) 73 (0.4–94.6) 285 (1–103.6) 249 (0.2–69.2) 198 (0.1–122.6) 11 (1.6–7.4) 5 (0.2–11) 6 (0.6–12.8)
71 74 57 39 39 54 79 85 75 65 69 76
(1.4–26.5) (7.4–31.5) (10–38.5) (18.2–43.8) (21–46.4) (27–44.6) (25–38.6) (25–35) (23.4–36) (16–35) (10–32) (4–24)
(49–98) (36–98) (27–90) (15–78) (17–66) (22–98) (46–98) (63–100) (61–98) (38–98) (42–94) (48–97)
Values are the mean of 4 years data (2010–2013). Values in parenthesis represent the minimum and maximum range.
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rate and severity of H. contortus infection (Getachew et al., 2007). The prevalence of H. contortus showed a definite seasonal trend that corresponds with the rainfall pattern in the study area. Maximum prevalence, mean intensity and abundance were recorded during rainy season while minimum during summer season which may be due to more availability of infective larvae (L3) on the pasture from where the animals acquire infection. Similar results have also been reported from Rajasthan (Singh et al., 1997), Maharashtra (Shirale and Made, 2007; Sutar et al., 2010), Assam (Bulbul et al., 2015; Hafiz et al., 2016), and Tamil Nadu (Varadharajan and Vijayalakshmi, 2015). These authors (loc.cit) suggested that environmental conditions during the rainy season are conducive for the development of infective larvae and high rainfall helps in larval dispersion on the herbage, which increases the chance of contact between host and parasite. Probably moderate temperature and high humidity during monsoon period may be more suitable for the development and survivals of infective stage of H. contortus. Rainfall may also help in the dispersion of larvae on pasture and thereby increases the chances of host’s contact with infective larvae (Katoch, 1998; Santos et al., 2012; Sanyal 1989a). Soulsby (1966) suggested that high rainfall during monsoon season provides suitable molarity of salts in the soil which enhance ecdysis and thereby transformation of L1 to L3 takes place easily. It is an established fact that the maximum growth of herbage occurs during rainy season, which may favour the survival and migration of larvae. Sanyal (1989b) studied the bionomics of pre-parasitic stages of ovine strongyle in faeces and on pasture and found that when there was sufficient rainfall, larvae were found to migrate vertically up to 15 cm and laterally up to 50 cm as compared to only 5 cm and 20 cm, respectively during non-rainy season. He further stated that infective larvae survive on pasture for more than 11 weeks in rainy season. Agyei and Amponsah (2001) and Silva et al. (2008) reported significant positive relationship between the level of infective larvae on herbage and rainfall. Higher temperature and rainfall cause stress to the host which lowers its immunity and predisposes it to a heavy infection (Hawkins, 1945). Low prevalence rate during summer and winter could be explained by the fact that these seasons are not conducive for the development of the infective larvae and therefore contamination of pasture were low. O’Connor et al. (2006) reported highest level of pasture contamination with free-living infective larvae (L3) during rainy while, lowest during dry season. The grass cover on the grazing pasture during dry season is reduced by which the eggs/larvae are exposed to desiccation, which either causes high mortality of larvae or they migrate deep into the soil (Ng’ang’a et al., 2004; Vlassoff, 1982). Urquhart et al. (1996) reported that the development of eggs become slow at low temperature and below 10 °C the development of L3 from eggs is stopped. It can be suggested from the present findings that 25–30 °C temperature, 75–85% relative humidity and more than 50 mm rainfall is more suitable for the development of infective stages of H. contortus. Similarly, Nahar et al. (2015) reported 29.8 °C temperature, 146 mm rainfall and 86% relative humidity are more suitable for larval development. O’Connor et al. (2006) reported that the development of eggs to infective larvae of H. contortus occur at 23–36 °C temperature and 70% relative humidity.
Table 2 Prevalence, mean intensity and abundance of Haemonchus contortus during different months of the year. Month
Number of animals examined
Number of infected animals
Prevalence (%)
Mean Intensity
Abundance
January February March April May June July August September October November December Total
49 44 49 50 58 58 51 60 52 50 53 61 635
12 14 18 20 32 26 38 58 47 43 38 37 383
24.48 31.81 36.73 40.00 55.17 44.82 74.50 96.66 90.38 86.00 71.69 60.65 60.31
75 88 93 128 324 264 526 786 640 588 438 306 354
18 28 34 51 178 118 391 759 578 505 314 185 263
Values are the mean of 4 years data (2010–2013).
found maximum. Although humidity was high (71–74%) in the month of January and February, prevalence was found very low which indicates that other factors like temperature and rainfall play a role in the prevalence. Variation in the mean intensity and abundance were also observed during different months. Highest values of these were found in August followed by September, while lowest values were recorded in January, February and March (Table 2). Mean intensity and abundance was found higher in those months which has moderate temperature (29 °C), high rainfall and maximum relative humidity. However, the values of both of these infection indices decline in those months which had extreme temperature either very low (13° C) or very high (35° C). Mean intensity and abundance showed a declining trend following the start of the dry spell from November. Statistical analysis of monthly data obtained for mean intensity and abundance by Kruskal-Wallis test, shows a highly significant difference in the mean intensity (KW = 45.24, p < 0.001) and abundance (KW = 46.13, p < 0.001). Analysis of Pearson’s correlation coefficient revealed that prevalence, intensity and abundance were positively correlated with the temperature, rainfall and relative humidity (Table 3). However prevalence, mean intensity and abundance were strongly related (r ≥ 0.6) with rainfall (p ≤ 0.05) and weakly related with temperature and humidity (r ≤ 0.1 − 0.5). 4. Discussion About 60% goats were found to be infected with H. contortus in Aligarh region. Similar results have also been reported from Kashmir valley (Tariq et al., 2008), Jammu region (Khajuria et al., 2013) and Meghalaya (Bandyopadhyay et al., 2010). Contrary to our findings either very high (70- 96%) or very low (6–36%) prevalence of H. contortus have been reported from many parts of India (Pathak and Pal, 2008; Sharma et al., 2009; Prakash and Bano, 2009; Mir et al., 2013). Such variation in the prevalence rate may be due to differences in the sample size, prevailing agro-climatic conditions, nutritional status and availability of susceptible hosts. As it has been reported that age, breed, nutrition and physiological state of the host influences the incidence
5. Conclusion H. contortus infections in goats at Aligarh, North India, showed a
Table 3 Prevalence, mean intensity and abundance of Haemonchus contortus during different seasons of the year. Seasons
Months
Number of animals examined
Number of infected animals
Prevalence (%)
Mean Intensity
Abundance
Summer Rainy Winter
Mar–Jun July–Sept Oct–Feb
215 163 257
96 143 144
44.18 87.18 54.92
202 650 299
95.25 576 210
Values are the mean of 4 years data (2010–2013).
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well-defined seasonal pattern. Rainfall seems to be the major limiting factor on the prevalence and worm burden as compared to temperature and humidity. The present findings may be used as a baseline data for developing an epidemiologically based control strategies for H. contortus in this region and may be helpful to stop indiscriminate use of anthelmintics. In the present study the effect of climatic factors on the survival of eggs/larvae was not studied, therefore, further studies are required.
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