Anthelmintic resistance, epidemiology and contlrol of gastrointestinal nematodes of small ruminants in Nyandarua district of Kenya and in Denmark
Abstract
Control of gastrointestinal nematodes in ruminants is most effectively achieved through
interventions based on the epidemiology of the parasites. Until recently, the epidemiology
of nematode infections in ruminants in most parts of Kenya had not been established. Lack
of this information for nematode infections in sheep in Nyandarua District of Kenya
necessitated epidemiological studies reported in this thesis.
No control programmes for nematodes of sheep in the area have previously been evaluated
and the effectiveness of a strategic control programme using closantel and albendazole and
based on the information from the epidemiological studies was therefore examined.
Anthelmintic resistance currently poses a senous threat to the effective control of
gastrointestinal nematodes particularly in small ruminants. A number of animal
management and worm control practices which are thought to enhance the selection 01"
worms resistant to anthelmintics have been identified. An understanding of the practices
contributing to the occurrence of resistance on a farm or region may assist in the design
of control programmes which limit the development and spread of resistance. There is
lack of this information for sheep and goat farms in Denmark and sheep farms in
Nyandarua District. An investigation was therefore undertaken to determine the prevalence
of anthelmintic resistance and factors contributing to its occurrence on these farms.
In the epidemiological studies in Nyandarua District, the prevalence and levels of infection
with gastrointestinal nematodes was monitored on 15 farms for a period of one year.
Haemonchus (55 %) and Trichostrongylus (23 %) were the most prevalent species in faecal
cultures and accounted respectively for over SO% and 35 % of the total worm burdens in
slaughtered sheep. Strongyle nematode EPG and pasture larvae infectivity were highest
(p <0.05) during the wet seasons. Strongyle EPG were highest in immature sheep (4-12
months old) throughout the year. These findings suggested that nematode control
programmes for sheep in the area should aim at minimising the high levels of infection,
particularly with H. contortus, during the wet season and reduce production losses from
subclinical infections during the dry season. Control should be targeted at the immature
sheep which carry the heaviest worm burdens. Adult sheep should also be treated
regularly as they contribute heavily to pasture contamination.
The effectiveness of strategic deworming with c1osantel, a long acting narrow-spectrum
anthelmintic, which is effective against Haemonchus in combination with albendazole, a
broad-spectrum anthelmintic, during the rainy seasons and albendazole during the dry
season in the control of gastrointestinal nematodes of sheep was investigated on a farm
in Nyandarua District. Levels of gastrointestinal nematode infections and pasture
infectivity were well controlled by the strategic treatments. This resulted in higher weight
gains, wool production, Pf'V, serum albumin and serum protein compared with untreated
sheep. These parameters were comparable between the strategic treatment group of sheep
and a group of sheep kept "worm-free" through treatments with albendazole every 3
weeks. A cost benefit analysis of the three strategies indicated monitory gains of US$ 14
and 13 per animal. in the strategic programme compared with those given suppressive
treatment and those in the control group respectively. It was concluded that worm control
strategies based on epidemiological inforrna' ion and the use of closantel and broad
spectrum anthelmintics could provide effective control of nematodes of sheep in the area
To obtain information on worm control practices with emphasis on the potential ris'
factors for the development of anthelmintic resistance, a questionnaire survey was carrie
out on 50 sheep farms in Nyandarua District and 183 sheep farms and 92 goat farms i
Denmark. The mean number of treatments per year in both countries were few, whic
implied less selection pressure for worms that are resistant to anthelmintics. However, j
Denmark, the majority of farmers interviewed (58 % for sheep farms and 52 % for go:
farms) did not follow predetermined drenching programmes and none of the 50 shec
farmers interviewed in Nyandarua District followed deworming programmes based on 0
epidemiology of the parasites. These treatments were therefore less likely to be effectiv
Underdosing which may enhance selection of worms that are resistant to anthelmintics
estimated to be common on farms in both countries. This was because the majority (84
and 69 % for sheep and goats, respectively in Denmark and 98 % for sheep in Nyandan
District) of farmers did not weigh adult animals but relied on visual appraisal to determi
body weights for drenching. This was also the case for lambs and kids on alar
proportion of farms (45 % and 41 %, respectively) in Denmark and for lambs on (
majority (96 %) of the farms in Nyandarua District. Only a small proportion (under 2('
in both countries) of the fanners used the recommended weight of the heaviest anini
in a group to calculate anthelmintic doses. One other factor identified on farms in br
countries which could enhance the selection of worms resistant to anthe1mintics was'
failure to follow Ole recommendation of alternating anthelmintics from different class
on an annual basis. This was observed on the majority of sheep farms (93 %) and goat
farms (85 %) in Derunark and sheep farms (97 %) in Nyandarua District.
The repeatability of responses obtained from 45 sheep farmers in Denmark in the
questionnaire survey was also examined through a second questionnaire interview. The
majority (72 %) of responses to variables on management practices were repeatable at least
to a fair degree. However, only 42 % of responses to variables on number of treatments
per year, drenching strategies and anthelmintic dosage determination had a fair to good
repeatability. There was aJso a decrease in repeatability associated with increasing time
to recall, when farmers were asked to give the identity of anthelmintics used during past
years. Although this investigation indicated that information obtained through the
questionnaire survey was fairly reliable, it highlighted the need to examine data quality
whenever questionnaires are used to obtain unrecorded information from farmers.
The occurrence of anthelmintic resistance was investigated on 16 sheep and 15 goat farms
in Denmark and 25 sheep farms in Nyandarua District using the Faecal Egg Count
Reduction Test (FECRT), the Egg Hatch Assay (EHA) for thiabendazole (TBZ) a
benzimidazole (BZ) and a Larval Development Assay (LDA) for TBZ, levamiso1e (LEV)
and ivermectin (rVM). The farms were selected from those responding to the
questionnaire survey.
Of the 16 sheep farms in Demnark, resistance to both LEV and IVM was found on 2
farms, to LEV on 2 farms, to BZs on 2 farms and to IV~1 on 1 farm using the FECRT.
For the goat farms, resistance to both BZ and LEV was found on 6 farms and to BZ am'
IVM on 1 farm. Resistance to BZ was also found on 2 farms and to LEV on 2 farms.
Ivermectin resistance was present on 1 farm. In Nyandarua District, resistance to both B
and LEV was found on 4 farms, to LEVan 3 farms and to BZ on 2 farms using th:
FECRI'. Although the number of farms examined were few, results of this investigatioi
revealed that resistance exists on farms in both countries. Steps to limit its developmen
and spread based on the factors identified in the questionnaire investigation therefore nee.
to be taken.
In the survey for resistance, the effects of using different methods of calculating the faecr
egg count reduction percentage (FECR %) in the FECRT was examined, Gras
disagreements in declaring resistance were observed between methods that utilis
geometric mean EPG and those that utilise the arithmetic mean EPG . Simil:
disagreements were observed between methods where only post-treatment EPG are usee
and those where both pre-treatment and post-treatment EPG are used. Inclusion or no)
inclusion of control group EPG also influenced the FECR % calculated. Results of th
investigation indicated that depending on the method used to calculate FECR %, for
particular farm, resistance may be declared or not. This could have significa
implications on the decision taken concerning the future use of an anthelmintic in tl
control of nematodes on a farm. The method of the World Association for e
Advancement of Veterinary Parasitology (WAA VP) appears least conservative
declaring resistance and may be the most suitable when monitoring resistance, to info:
fanners of the slightest change in the efficacy of an anthelmintic.
Finally, the relationship between resistance detected in the FECRT and the lethal dose
50% (LD50) in the EHA and the LDA was examined for the data obtained from 13 sheep
farms and 12 goat farms in Denmark. The majority (90%) of the farms declared resistant
to BZ according to the FECRT had LD50 values above 0.5 p,M TBZ (0.1 p.g TBZ/mI)
in the EHA, indicating resistance. Majority of these farms were those having goats. One
third of the isolates declared susceptible to BZ in the FECRT were resistant according to
the EHA (LD50 >0.5 p,M TBZ). There were also disagreements in declaring BZ c,
resistance between the LDA and both the FECRT and EHA on 40 % and 45 % of the
farms, respectively. Groups of farms declared resistant to LEV according to the FECRT
had higher mean LD50 values compared to those declared susceptible to LEV. However,
only 4 out of 12 farms declared resistant to LEV had LD50 values higher than 1.2p,M
LEV (0.28 p,g LEV/m!) recorded previously for a LEV-susceptible strain of Ostertagia
circumcincta. This indicated discrepancies in declaring resistance to LEV between the
FECRT and the LDA. There was agreement in declaring resistance to Iv M between the
FECRT and the LDA. It was concluded that the sensitivity of the three tests used needs
to be improved or alternative and more specific methods of detecting anthelmintic
resistance established.
Citation
Doctor of Philosophy degreePublisher
University of Nairobi Department of Veterinary Pathology & Microbiology