Veterinary Parasitology 198 (2013) 244–249

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Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar

Short communication

Effect on performance of weanling alpacas following

treatments against gastro-intestinal parasites
Susan M. Thomas a,b,∗ , Eric R. Morgan a
a
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, United Kingdom
b
Pathology & Pathogen Biology (PPB) Hawkshead, The Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield,
Hertfordshire AL9 7TA, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: Nematodes and coccidia are common parasites of alpacas (Vicugna pacos), and important
Received 8 July 2013 causes of disease in this increasingly popular livestock species. Endoparasitic infestation is
Accepted 12 August 2013
thought to increase at times of natural or imposed stress, and antiparasitic treatments are
often administered, although to date there is little evidence regarding their effect. Thirty-
Keywords:
one alpaca juvenilles (cria) were divided into four groups at weaning, and received either
Alpaca
no treatment as a control (C), fenbendazole anthelmintic (FB), toltrazuril coccidiostat (T), or
Coccidiosis
Nematode both treatments (FBT). Body weights and faecal egg/oocyst counts were recorded weekly
Parasite for six weeks following treatment. Although the prophylactic treatments decreased fae-
Toltrazuril cal egg/oocyst counts of the target organisms in the short term, there was no significant
Fenbendazole difference in egg/oocyst output over the course of the trial from animals given wormer, coc-
cidiostat or both treatments. The group receiving anthelmintic only showed a significant
reduction in live weight gain (LWG), with no significant difference in LWG between the
other groups. At the conclusion of the trial, ‘wormed only’ alpacas weighed 3.3% less than
at weaning, losing an average 1.3 kg over six weeks, whereas average LWG in the control
group was 2.5 kg. Antiparasitics transiently reduced egg/oocyst output but results suggest
that further investigation is required on the action of anthelmintics administered to alpaca
cria at weaning and their effect on animal health and welfare.
© 2013 Elsevier B.V. All rights reserved.

1. Introduction (Wheeler, 1995), parasitic disease is cited as the main herd

health problem (Palacios et al., 2006). Nematode infesta-
Alpacas, members of the South American Camelid fam- tions are common and are reported to have the largest
ily (SAC’s) are an increasingly popular livestock species impact, particularly on alpacas aged less than one year
outside their home range, with >35,000 alpacas farmed (Leguia, 1991). Ballweber (2009) reports that parasitism
in the UK (British Alpaca Society (BAS) 2012, personal is a major health concern in SAC’s, throughout the world,
communication). Published research on alpacas reared in with clinical disease causing severe economic losses. A
Europe is scarce, prompting the need for more evidence postal survey of camelid owners in the UK reported that
based information for husbandry and parasite control. 93% of owners treated their alpacas or llamas for nema-
In Peru, where there are more than 4 million alpacas todes, and 20% treated for coccidia (Tait et al., 2002).
Research in Germany identified that cria demonstrated
higher strongyle egg counts (average 450 eggs per gram,
∗ Corresponding author at: Pathology & Pathogen Biology (PPB) Hawk-
epg) than adults (150 epg), and eggs of Nematodirus bat-
shead, The Royal Veterinary College, Hawkshead Lane, North Mymms,
tus and other Nematodirus spp., Strongyloides, Trichuris,
Hatfield, Hertfordshire AL9 7TA, United Kingdom. Tel.: +44 7887 511774. Capillaria and Moniezia were repeatedly recovered dur-
E-mail address: smthomas@rvc.ac.uk (S.M. Thomas). ing a year of sampling (Rohbeck et al., 2006). A study

0304-4017/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.vetpar.2013.08.010
 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249 245

including faecal analysis in the UK, identified a range of having attained an age of at least five months and a
endoparasites including Ostertagia, Haemonchus, Cooperia, minimum weight of 25 kg. A random number genera-
Trichostrongylus sp, Nematodirus, Capillaria and Trichuris tor allocated a number to each cria which was used to
(Tait et al., 2002). A similar range of gastrointestinal nema- assign individuals to one of four test groups (C- control,
tode eggs was identified in a study in the USA (Bishop FB- fenbendazole anthelmintic, T- totrazuril coccidiostat
and Rickard, 1987). The highest numbers of nematode and FBT-both fenbendazole and toltrazuril). The weanling
eggs were found in cria, possibly due to the more limited alpacas were moved onto 5 acres of pasture where they
opportunity of juveniles to develop immunity. While many were co-grazed. To minimise contamination from previ-
species of gastro-intestinal parasites are shared between ously shed parasite eggs the pasture had been cleared of
SAC and ruminants, the nematodes Camelostrongylus men- faecal deposits 16 months prior to the trial and had been
tulatus and Trichuris tenuis are unique to camelids (Fowler, managed by taking a cut of hay during the summer. They
1997). These species were reported in the UK following weanlings were given access to three automatically fill-
post mortem recovery from alpaca and llama cria, respec- ing drinking butts of fresh water which were raised from
tively (Welchman et al., 2008). Nematode infections reduce the ground to minimise contamination from mammalian
alpaca productivity both in terms of fleece production and wildlife. Three mangers of hay were available for ad libi-
weight gains. Infection with protozoal Eimeria species is tum feeding. Commercial camelid hard feed was presented
reported to be the main cause of mortality in young alpaca daily in 6 m × 3 m lengths of raised guttering, as was the
in Peru (Palacios et al., 2006). There are six recognised coc- practice prior to weaning, providing each cria ample space
cidia species specific to SAC, Eimeria alpacae, E. lamae, E. to approach the trough with minimal competition for feed.
macusaniensis, E. punoensis, E. peruviana and E. ivitaensis Faecal testing of cria prior to weaning identified the
(Soulsby, 1982; Leguia and Casas, 1998; Fowler and Miller, main helminth eggs as Nematodirus battus, strongyles
2008). Analysis of coccidiosis presenting at post mortem in (H.contortus, and Trichostrongylus spp) and Trichuris spp.
54 UK alpaca from 1999 to 2004 concluded that coccidial (mean total nematode egg counts of 52 epg, range 0–200).
infection, particularly associated with E. macusaniensis and Coccidia species identified were E. alpacae, Eimeria macu-
E. punoensis cause disease in British alpaca over a wide age saniensis and Eimeria ivitaensis (mean counts 47 opg, range
range (Schock et al., 2007). 0–400) Cria were weighed at the start of the trial for dosage
Signs of parasitism vary. Cria are particularly vulnerable, calculations. No antiparasitic drugs are licensed in the UK
possibly due to immature immune development and also for alpacas, so treatments were selected on the basis of
due to the reduced nourishment available from a lactating the main parasite ova present. Drugs and doses adminis-
dam if she is also parasitised (Fowler, 1998). Windsor et al. tered were those in common current use in the camelid
(1992) found that parasite infection reduced weight gain industry. Recommended doses range between 2 and 4
in growing alpacas, and, importantly from the commer- times sheep dose for both FB anthelmintic and coccidio-
cial perspective, treated male alpacas produced a greater stats (Whitehead and Anderson, 2006; Whitehead, 2009).
fleece yield. Key events (birthing, lactation and weaning) A recent study focussing on another SAC, the llama (Lama
when increased stress is linked to depressed immune sta- glama) demonstrated that dose rates of 7.5 mg/kg BW were
tus may lead to rises in egg and oocyst counts; treatments required to reduce egg shedding of gastrointestinal nema-
with anthelmintics and coccidiostats are often initiated. todes in contrast to a dose rate of 2.5 mg/kg to achieve
Cria are weaned at approximately six months of age, having similar results in sheep (Dadak et al., 2013). It was hypo-
reached 25 kg in weight. As the majority of UK cria births thesised that the three fold increase was required due to
are timed for summer, weaning is typically performed in pharmokinetic differences between species.
winter. Cria are removed from the dam and the protec- According to group, alpacas were given either no treat-
tion of the herd onto relatively poor quality winter grass ment (group C, n = 8) or the allocated group treatments
at a time when the weather becomes cooler and wetter. of fenbendazole (15 mg per kg body weight as a single
This can impose physiological and nutritional stress, which oral dose of 1.5 ml per 10 kg body weight of Panacur 10%
may be exacerbated by parasite infection, so the benefit of suspension, MSD Animal Health, UK, i.e. triple the recom-
antiparasitic treatment at this time is plausible. However, mended sheep dose; group FB, n = 8), toltrazuril (15 mg per
evidence for such a benefit has not been published. kg body weight as a single oral dose of Baycox 50 mg/ml
The aim of this study was to examine the effects oral suspension, Bayer plc, corresponding to 3 ml/10 kg;
of administering the antiparasitic drugs fenbendazole group T, n = 8) or fenbendazole followed immediately by
(anthelmintic) and/or toltrazuril (coccidiostat) to cria at toltrazuril (group FBT n = 7). Drenches were administered
weaning to assess the level of egg/oocyst shedding and the over the back of the tongue in the normal milk feeding
effect on weaning performance measured by live weight position and a swallowing reflex encouraged to avoid the
gain (LWG). drench spit back. Each alpaca was handled in the same way,
whether they received an oral drench or no medication, to
2. Materials and methods ensure that all alpacas were exposed to the same degree of
handling and stress.
The study was carried out over a seven week period At the start of the trial (week zero), and weekly there-
beginning in January 2011 on a closed alpaca farm (120 after, cria were individually assessed for body condition,
alpacas) in south-west England. A factorial, randomised weighed and observed for clinical signs of illness. Faecal
controlled trial was designed using a group of 31 sum- egg counts were conducted using the modified McMaster
mer born alpaca cria. The group satisfied weaning criteria test at a detection limit of, 50 eggs or oocysts per gram of
246 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249

Fig. 1. Faecal nematode egg counts recovered from 4 treatment groups, treated with anthelmintic (0 = untreated, 1 = treated) and coccidiostat (0 = untreated,
1 = treated) monitored from weaning week 0 to week 6. N = 8 in groups C, FB, and T, n = 7 in group FBT. Each box represents 50% of the cases with the whiskers
extending to the largest and smallest values. Horizontal lines within the box represent median values. Extreme points are represented by asterisks.

faeces (epg, opg), (Zajac and Conboy, 2006) and Sheather’s opg (2 (3 d.f., n = 31) = 6.85, p = 0.077). Positive weight
sugar flotation solution (specific gravity 1.27). Sheather’s gains were recorded in groups C, T and FBT (Fig. 3). Group
was selected as flotation medium as it will float both nema- FB, demonstrated the lowest LWG compared with other
tode eggs and the relatively large Eimeria oocysts of Eimeria groups (F3,27 = 5.88 p = 0.022). Neither groups T or FBT had
macusaniensis and E. ivitaensis. a statistically significant effect on LWG relative to the con-
The effect of treatment on epg and opg was evaluated. trol group (p = 0.55 and p = 0.48 respectively). Mean LWG
The principal indicator of weaning performance through- over the six week trial in C was 2.5 kg, T was 1.7 kg and in
out the trial was live weight gain (LWG). To remove FBT was 0.7 kg, Alpacas in group FB, lost on average 1.3 kg.
the effect of variation in cria weaning weights, initial
weights were indexed to 1. As weight data were normally
distributed, they were analysed using a mixed between- 4. Discussion
within subjects repeated measures ANOVA to determine
the effects of anthelmintic or coccidiostat treatment on Anthelmintic and coccidial treatment had the expected
LWG, exploring any interaction effects. Statistical analy- effect of reducing numbers of nematode eggs and coccidial
ses were performed using PASW v18.0 (SPSS Inc., USA) oocysts shed onto the pasture following weaning. However
with alpha = 0.05, except when repeated univariate com- the effects of treatment were transient with numbers of
parisons were made, in which case Bonferroni adjustment ova shed returning to pre-treatment levels by week 4 and
was applied. 5 of the trial. Re-infection from the pasture was unlikely
as the trial pasture had been managed and ungrazed for
>1 year prior to the trial. Survival of L3 on pasture varies
3. Results both between species and with environmental conditions,
but it is unlikely that larvae would have survived in high
Groups FB and T showed significant reductions in numbers both a hot dry summer and adverse freezing win-
total egg/oocyst counts for the first 3 weeks of the trial ter conditions (Kates, 1950). Given the speed of return to
Figs. 1 and 2 and both treatments were well tolerated by pre-treatment egg counts (4–5 weeks post treatment) it is
the cria. plausible that eggs were shed by recently emerged arrested
Faecal egg and oocyst counts in treated groups returned larvae (L4) rather than re-infection from previously cleaned
to untreated levels by weeks 4 and 5 such that there was no and rested pasture. However, given the limited infor-
significant difference over the entire trial period in either mation available on antiparasitic drug efficacy against
epg (Kruskal–Wallis 2 (3 d.f., n = 31) = 6.59, p = 0.086) or the various parasites found in alpacas, and the limited
 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249 247

Fig. 2. Faecal oocyst counts recovered from 4 treatment groups, treated with anthelmintic (0 = untreated, 1 = treated) and coccidiostat (0 = untreated,
1 = treated) monitored from weaning week 0 to week 6. N = 8 in groups C, FB, and T, n = 7 in group FBT. Each box represents 50% of the cases with the
whiskers extending to the largest and smallest values. Horizontal lines within the box represent median values. Extreme points are represented by
asterisks.

opportunities for specific identification of eggs and oocysts accurate dose based on weight. 75% of alpaca herds in the
shed in the present study, it is also possible that post- UK comprise <20 alpacas (BAS data, 2012). Such small hold-
treatment increases in epg and opg represent emergence ings rarely own farm scales adequate to weigh an alpaca
of species that were less affected by treatment or oth- (2012 on-line survey, unpublished data). Animal weights
erwise held a competitive advantage. Whilst combined are often estimated visually, which is prone to error with an
oocyst counts in the two groups given coccidiostat were alpaca in full fleece. This could lead to sub-optimal dosing
lower than the untreated groups, numbers of oocysts shed promoting development of anthelmintic resistance.
returned to untreated levels by week 5 following wean-
ing (although there was a temporary increase in week 3,
group T). Studies have shown continued suppression of 1.10
Group mean weight Index - Weaning weight = 1.00

oocyst levels for several weeks following treatment with 1.08

toltrazuril, which destroys all intracellular stages of the
1.06
Eimerian life cycle (Mundt et al., 2007).
With no licenced antiparasitic drugs for SAC’s there 1.04
is doubt regarding optimal dose rates for treatments, 1.02
which rely on the application of approaches developed for
1.00
distantly related species, usually with no validation. Ris-
ing levels of anthelmintic resistance in ruminants must 0.98
raise concerns for alpaca herds. Anthelmintic resistance in 0.96
alpacas to macrocyclic lactone (ML) anthelmintics has been
0.94
demonstrated on an alpaca farm in Belgium (Sarre et al.,
2012) in spite of a rotational worming strategy between 0.92
ML and benzimidazole (BZ) treatments. Gillespie et al. 0.90
(2010) identified resistance to BZ (fenbendazole) and ML 0 1 2 3 4 5 6
(ivermectin and moxidectin) on alpaca and llama farms Weaning Week
in Georgia, USA. Alpacas in the UK are routinely treated C FB T FBT
against nematodes, and this can vary from twice each year
Fig. 3. % weight change (±SE) as a summary measure of 4 treatment
to six times a year (2012 on-line survey, unpublished data).
groups over 6 week trial period. Initial weights were indexed at 1 to
Reported treatment dosages vary from sheep dose rates to normalise start point weaning weights and percentage changes were cal-
up to 4x sheep dose rates. Effective treatment relies on an culated weekly.
248 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249

LWG was affected by treatment but not in the direc- inflicting no harm. The current research was undertaken on
tion anticipated. The group treated with anthelmintic alone a single holding with relatively small numbers of animals,
(FB) lost weight over the trial period while all other groups although the unexpected outcome suggests more research
demonstrated weight gain. This suggests that removal of is warranted.
worms created an adverse environment in the gut which
had the effect of either reducing appetite or reducing effi-
Acknowledgements
ciency of nutrient absorption, utilisation, or both. The effect
appeared to be attenuated in FBT, where LWG was positive
The authors thank Sheelagh Lloyd and Richard Wall for
over six weeks but at lower levels than groups C and T. Fur-
valuable comments on an earlier draft.
ther research is required as this unexpected outcome has
not been explained.
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