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New Zealand Veterinary Journal
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Clinical efficacy and tolerance of an extract of
green-lipped mussel (Perna canaliculus) in dogs
presumptively diagnosed with degenerative joint
disease
B Pollard a , WG Guilford a , KL Ankenbauer-Perkins b & D Hedderley c
a Institute of Veterinary, Animal and Biomedical Sciences , Massey University , Private
Bag 11222, Palmerston North, New Zealand E-mail:
b Estendart Ltd , Palmerston North, New Zealand
c New Zealand Institute of Crop and Food Research Ltd , Palmerston North, New Zealand
Published online: 18 Feb 2011.
To cite this article: B Pollard , WG Guilford , KL Ankenbauer-Perkins & D Hedderley (2006) Clinical efficacy and tolerance
of an extract of green-lipped mussel (Perna canaliculus) in dogs presumptively diagnosed with degenerative joint disease,
New Zealand Veterinary Journal, 54:3, 114-118, DOI: 10.1080/00480169.2006.36622
To link to this article: http://dx.doi.org/10.1080/00480169.2006.36622
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Scientifi c Article
Clinical ef cacy and tolerance of an extract of green-lipped mussel
(Perna canaliculus) in dogs presumptively diagnosed with
degenerative joint disease
B Pollard*, WG Guilford*§, KL Ankenbauer-Perkins† and D Hedderley‡
Abstract
AIM: To evaluate the effi cacy and tolerance of an extract of
green-lipped mussel (GLME) in the management of mild-to-
moderate degenerative joint disease (DJD) in dogs.
METHODS: Eighty-one dogs presumptively diagnosed with
DJD were treated orally daily with either GLME or a placebo
for 56 days, in a double-blind, placebo-controlled study. In an
uncontrolled open-label extension to the study, all dogs were
treated with GLME for an additional 56 days (from Days 57–
112). Clinical signs were subjectively scored by the owners, and
fi ndings of detailed musculoskeletal examinations were scored
by one veterinarian. Effi cacy was assessed from a qualitative
comparison of the proportion of dogs with improved clinical
signs, and a quantitative comparison of the scores of the mus-
culoskeletal examinations, between groups. Haematological and
biochemical analyses and reports by owners of possible adverse
drug reactions were used to screen for evidence of toxicity.
RESULTS: There was close agreement between assessments by
the veterinarian and owners. The clinical signs of DJD in both
GLME-treated and placebo groups improved signifi cantly over
baseline by Day 28; this improvement continued over the en-
tire course of the study. There were no signifi cant differences
between groups on Day 28. On Day 56, a higher proportion
of dogs in the GLME-treated group had improved clinical
signs (p=0.018), and GLME-treated dogs had marginally bet-
ter (p=0.053) musculoskeletal scores than dogs in the placebo
group. The differences between the groups were no longer ap-
parent by Day 112, by which time the former placebo group
had been receiving GLME for 56 days in the open-label phase of
the study. The proportion of dogs in the former placebo group
that had improved by Day 112 (29/32; 91%) was signifi cant-
ly greater (p=0.012) than the proportion improved at Day 56
(15/37; 41%). No signs of toxicity were apparent.
CONCLUSIONS AND CLINICAL RELEVANCE: GLME had
a benefi cial effect on the clinical signs of dogs presumptively di-
agnosed with mild-to-moderate DJD. Long-term therapy may
be required before improvement is apparent.
KEY WORDS: Green-lipped mussel extract, Perna canaliculus, de-
generative joint disease, arthritis, dog
Introduction
Degenerative joint disease (DJD) or osteoarthritis is the most fre-
quently diagnosed arthropathy of animals (Pedersen et al 2000).
The cause of DJD is unknown but numerous predisposing factors
have been recognised. These include obesity, instability, laxity or
malalignment of joints, trauma, excessive work, and genetic fac-
tors (Smith et al 1995, 2001; Pedersen et al 2000). The predispos-
ing factors result in accelerated turnover of the articular cartilage
matrix, which eventually leads to localised degeneration of articu-
lar cartilage, exposure and sclerosis of underlying bone, formation
of osteophytes, and thickening of the synovia (Manley 1995; Ped-
ersen et al 2000). Damage to the articular cartilage is mediated
by cytokines, prostaglandins, proteinases and oxygen-derived free
radicals (Manley 1995). Eventually, the cumulative damage to the
joints leads to clinical signs such as unwillingness to exercise, re-
stricted joint movement, pain, stiffness, lameness, and crepitation
or joint thickening (Manley 1995; Pedersen et al 2000).
The diagnosis of DJD is based on the history and clinical signs,
as well as radiography of affected joints. Radiography will not
detect early cartilage degeneration but will reveal more advanced
degenerative changes such as osteophyte formation, subchondral
sclerosis, attrition of subchondral bone, joint deformity and sub-
luxation (Pedersen et al 2000). In certain clinical presentations,
other diagnostic steps such as evaluation of joint fl uid, synovial
biopsy and tests for rheumatoid factor are indicated to diagnose
less common forms of joint disease such as septic arthritis, im-
mune-mediated polyarthritis and rheumatoid arthritis. However,
evaluation of synovial fl uid per se does not have suffi cient sensitiv-
ity or specifi city to allow clinicians to reach a defi nitive diagnosis
of DJD (Gibson et al 1999; Pedersen et al 2000).
Traditionally, treatment of DJD has centred on rest, controlled
exercise, management of predisposing factors, and periodic use of
non-steroidal anti-infl ammatory agents to reduce synovial infl am-
mation and pain (Manley 1995; Pedersen et al 2000). The search
for compounds to relieve the symptoms and alter the course of
osteoarthritis has ranged across a wide spectrum of botanical,
zoological, chemical and manufactured materials. This search for
compounds showing the ideal balance between effi cacy, side-ef-
fects and cost continues unabated. Recently, there has been an
upsurge in interest in chondro-protective agents and alternative
therapies such as parenterally-administered polysulphated gly-
cosaminoglycans, and a variety of dietary supplements including
* Institute of Veterinary, Animal and Biomedical Sciences, Massey University,
Private Bag 11222, Palmerston North, New Zealand.
† Estendart Ltd, Palmerston North, New Zealand.
‡ New Zealand Institute of Crop and Food Research Ltd, Palmerston North,
New Zealand.
§ Author for correspondence. Email: w.g.guilford@massey.ac.nz
ANOVA Analysis of variance
DJD Degenerative joint disease
GLME Green-lipped mussel extract
SD Standard deviation
New Zealand Veterinary Journal 54(3), 114-118, 2006 114
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anti-oxidants, chondroitin sulphate, glucosamine, omega-3 fatty
acids, milk protein concentrate, and GLME (De Haan et al 1994;
Gingerich and Strobel 2003).
GLMEs are derived from the New Zealand green-lipped mus-
sel (Perna canaliculus). Various types of GLME have been em-
ployed in the management of arthritis. These include stabilised
freeze-dried powdered preparations of the mussel tissue and oily
extracts. Some authors observed a benefi cial effect of GLME on
rheumatoid arthritis and osteoarthritis in humans (Gibson et al
1980; Gibson 2000) but others did not (Larkin et al 1985; Dar-
lington and Stone 2001). In dogs, recent studies by Bui and Bierer
(2001) demonstrated that the addition of a green-lipped mussel
powder to a dry diet resulted in signifi cant clinical improvement
in arthritis by the end of 6 weeks of treatment. In contrast, a lower
dose of green-lipped mussel powder did not result in clinical im-
provement in another study of arthritis in dogs (Dobenecker et
al 2002).
The purpose of the placebo-controlled phase of the study present-
ed here was to compare the effi cacy of a GLME with a placebo
in alleviating the clinical signs of mild-to-moderate canine DJD.
A secondary objective was to evaluate the tolerance of the GLME
by dogs. The objective of the open-label phase of the study was to
provide the manufacturer of the GLME-containing product with
commercially-relevant information on the effi cacy of the product
as perceived by pet owners.
Materials and methods
Dogs
The 81 dogs (43 in the treated group and 38 in the placebo group)
used in the study were selected from lame dogs presenting over a
10-month period to the Veterinary Teaching Hospital, Massey
University, Palmerston North, New Zealand, or to private veteri-
nary clinics in the lower North Island of New Zealand. The dogs
all had clinical histories consistent with DJD, including intermit-
tent or continuous lameness, stiffness on rising, and diffi culty
walking up or down stairs. The dogs remained in their owners’
care for the duration of the study. The study was approved by the
Massey University Animal Ethics Committee, Palmerston North,
New Zealand.
Diagnostic procedures
The dogs were confi rmed as generally healthy, following physical
examination and routine urine, haematological and biochemical
analyses. All dogs underwent a musculoskeletal examination con-
ducted by the same veterinarian, to identify the affected joint(s).
Radiography was performed to help confi rm the diagnosis of DJD
and rule out other causes of lameness. Joint taps were not per-
formed on the dogs selected into the study because the procedure
was not considered to be clinically indicated. Specifi cally, the dogs
did not have a history or clinical signs suggestive of polyarthritis
or septic arthritis, and there are no known tick-borne arthroses in
dogs in this geographic region.
Criteria for selection and allocation of cases
Dogs presumptively diagnosed with mild-to-moderate DJD of
more than 1 month’s duration were considered for inclusion.
Results of musculoskeletal examinations were graded using a
scale of 1–5 (score increasing with increasing severity) proposed
by Holtsinger et al (1992) for each of fi ve parameters: lameness,
weight-bearing, joint mobility/palpation, willingness to hold up
the contra-lateral limb, and pain (Table 1). Dogs were excluded
if they had a score >4 in one or more of these lameness grading
categories, or if they had clinical evidence of septic or immune-
mediated arthritis, neurological disorders, bleeding disorders, or
were pregnant. Dogs were also excluded if they had been treated
with topical or systemic anti-infl ammatory agents (including oral
nutritional supplements containing GLME) within the previ-
ous 2 weeks, with intra-articular injections within the previous
3 months, or had undergone orthopaedic surgery of any type
within the previous month.
Dogs entering the study were grouped according to the joint(s)
primarily affected (hip, shoulder, stifl e, or other) and randomly
allocated to one of two groups, viz treatment with a product con-
taining GLME, or treatment with a placebo.
Treatment
The GLME treatment (SF4 Dog; McFarlane Laboratories New
Zealand Ltd, Auckland, NZ) contained 125 mg GLME per tab-
let, 52.86 mg brewer’s yeast, 191.50 mg lactose and 10.64 mg tab-
Table 1. Grading scale used by a veterinarian to assess the severity
of musculoskeletal dysfunction in dogs presumptively diagnosed with
degenerative joint disease (modifi ed from Holtsinger 1992).
Parameter Grade Signs/assessment
Lameness
1 Stands and walks normally
2 Stands and walks normally, slight lameness
at the walk
3 Stands normally, severe lameness at the walk
4 Abnormal posture when standing, severe
lameness at the walk
5 Reluctant to rise and will not walk >5 strides
Willingness to hold up contra-lateral limb
1 Readily accepts for >2 min
2 Mild resistance, accepts for >1min
3 Moderate resistance, replaces it in <30 sec
4 Strong resistance, replaces it in <10 sec
5 Refuses to raise contra-lateral limb
Weight-bearing
1 Normal weight-bearing
2 Normal weight-bearing at rest, favours limb
when walking
3 Partial weight-bearing at rest and at the walk
4 Partial weight-bearing at rest, non-weight-
bearing at the walk
5 Non-weight-bearing at rest and when walking
Pain
1 No pain elicited on palpation of affected joint
2 Mild pain on palpation, e.g. turns head
3 Moderate pain on palpation, e.g. pulls limb away
4 Severe pain on palpation, e.g. vocalises,
attempts to bite
5 Will not allow examiner to palpate joint
Joint mobility/palpation
1 No limitation of joint motion, no crepitus
2 Mild (10–20%) decreased range of motion, no
crepitus
3 Mild (10–20%) decreased range of motion,
crepitus
4 Moderate (20–50%) decreased range of motion,
crepitus
5 Severe (>50%) decreased range of motion,
crepitus
115 New Zealand Veterinary Journal 54(3), 2006 Pollard et al
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leting aid (magnesium stearate, acacia and aerosil). The placebo
contained the same ingredients except for the GLME which was
replaced by dried fi n-fi sh (McFarlane Laboratories Ltd), and was
of similar size, shape, colour, and odour to the GLME treatment.
Both types of tablet were provided in identical plastic screw-top
bottles identifi ed only by code numbers. Both tablets were of a
size easy to administer, were highly palatable to the dogs, and were
administered daily according to bodyweight, viz 5–15 kg (three
tablets), 16–20 kg (fi ve tablets), 21–25 kg (six tablets), 26–45 kg
(eight tablets), and 46–65 kg (nine tablets). Owners recorded the
treatment and any observations of note in a daily log. Treatment
continued for 56 days. Owner compliance was checked by re-
viewing the daily log and counting the tablets remaining in the
bottles at the end of the treatment period.
At the conclusion of the placebo-controlled study, the owners
were offered an open-label extension to the trial during which
all dogs were treated with the GLME-containing product for 56
days. Thus, at the conclusion of the open-label phase of the trial,
half the dogs had received GLME for 112 days and half had re-
ceived GLME for 56 days.
Clinical examinations and sampling
The dogs were evaluated by the same veterinarian prior to com-
mencement of treatment and after approximately 28, 56, and 112
days. Assessments at those intervals included a general physical
examination and a musculoskeletal examination, scored as de-
scribed above.
Blood samples were collected prior to treatment and on Day 56,
by cephalic or jugular venepuncture. Samples collected into tubes
containing EDTA were used for a complete blood count, includ-
ing numbers of platelets. Serum was harvested in plain blood
collection tubes, for analysis of the concentrations of calcium,
phosphorus, sodium, potassium, bicarbonate, chloride, urea, cre-
atinine, bilirubin, cholesterol, total protein, albumin, and globu-
lin; the anion gap and albumin/globulin ratio; and the activity
of creatine phosphokinase, aspartate aminotransferase, alanine
aminotransferase, amylase, and lipase. Urinalysis was performed
on free-catch urine. All analyses were performed by a commercial
animal health laboratory (Batchelar Animal Health Laboratory,
Palmerston North, New Zealand), and data were compared to the
established reference ranges of that laboratory.
Assessments by owners
The general health of the dogs (appetite, attitude, level of activity,
faecal consistency, and the presence of vomiting or any other ab-
normalities) and severity of lameness were assessed by their own-
ers on Days 0, 26, 52 and 112. These assessments were recorded
on forms using visual analogue and ordinal grading scales. Own-
ers were also asked for an overall assessment as to whether or not
their animal’s condition had or had not improved.
Musculoskeletal assessment by the veterinarian
The severity of each dog’s musculoskeletal dysfunction was as-
sessed in both quantitative and qualitative manners. The fi ve
musculoskeletal parameters considered were assessed in a stand-
ardised way at each examination and a score for each parameter
was allocated (Table 1). The scores of the individual parameters
were added to give a cumulative score for each musculoskeletal
examination. The cumulative score at each assessment during the
trial was used as the quantitative clinical assessment. At each ex-
amination, the quantitative clinical assessment was qualitatively
categorised as ‘improved’ (i.e. cumulative score lower than previ-
ous examination) or ‘not improved’. This qualitative clinical as-
sessment was based on the change (if any) in the cumulative score
over baseline (Day 0).
Assessment of tolerance
Tolerance of the treatment was assessed by a comparison of the
owners’ reports of any adverse effects of the GLME treatment and
placebo, and a review of the haematological, serum biochemistry
and urinalysis data.
Statistical analysis
All statistical analyses were performed using SAS for Windows,
v6.12 (SAS Institute Inc, Cary NC, USA). The degree of agree-
ment between the owners’ assessments of improvement and the
veterinarian’s qualitative assessment of improvement on Days
0, 28, 56 and 112 were analysed using the Kappa statistic. The
veterinarian’s qualitative assessments of improvement of the two
groups of dogs on Days 0, 28, 56 and 112 were compared using
logistic regression.
The cumulative musculoskeletal scores of the two groups were
compared over Days 0, 28, 56 and 112, using repeated measures
analysis of variance (ANOVA). Only complete datasets from dogs
that had been examined on all four occasions were used for this
analysis. The distribution of the residuals was checked for normal-
ity and homogeneity of variance; these checks confi rmed that the
assumptions of ANOVA applied to the cumulative scores. Con-
trasts were used to test whether there was any signifi cant change
between successive observations.
Results
Case recruitment
One hundred and forty-two dogs were presented for this study
and of these 84 met the inclusion criteria. Data from three of
these were eventually excluded from analysis as one dog was di-
agnosed with osteosarcoma of the scapula towards the end of the
trial and the owners of the other two dogs failed to comply with
the experimental protocol. Thus, data from 81 dogs were includ-
ed in statistical analyses.
The mean age of the dogs was 8.5 (SD 3.3) years and mean
weight was 32.6 (SD 11.1) kg. There were 48 females (59%), and
the most common breeds were Labrador Retriever (26%), Ger-
man Shepherd dog (12%), Border Collie (11%), and Rottweiler
(11%).
The majority of the 81 dogs included in the data analysis com-
pleted the study. Seven of the 81 dogs did not complete the study
for the following reasons, but partial datasets from these dogs were
available. Three dogs were euthanised during the study: a 13-year-
old dog in the GLME-treated group and an 11-year-old dog in
the placebo group were euthanised due to overall poor quality of
life, and an 11-year-old dog in the placebo group was euthanised
for renal failure. Two dogs in the GLME-treated group and two
in the placebo group were formally withdrawn from the study.
Of these four, one owner believed the treatment caused the dog’s
coat to smell (this dog was in the placebo group), one dog in
the treated group required anti-infl ammatory treatment, and two
owners were unable to continue to participate in the study. Data
were incomplete from another four dogs because one dog was not
presented for examination on Day 28, one was not presented on
Day 56, and two animals were not presented on Day 112.
Pollard et al New Zealand Veterinary Journal 54(3), 2006 116
Downloaded by [FU Berlin] at 04:34 03 December 2014
The DJD of the dogs included in the study most frequently af-
fected the hip joint (43%) followed by the stifl e (16%) and shoul-
der (10%).
Agreement between assessments by the veterinarian and
owners
Agreement between the owners’ assessments of improvement and
the veterinarian’s qualitative clinical assessments was 78% on Days
28 and 56, and 91% on Day 112, when both groups were treated
with the GLME-containing product. The corrected coeffi cient of
agreement (Kappa) was 0.546 on Day 28, 0.547 on Day 56, and
0.698 on Day 112, and there was no sign of systematic bias.
Qualitative clinical assessment
Results of the qualitative clinical assessments are shown in Table 2.
On Day 28, there was no signifi cant difference between the pro-
portion of dogs showing improvement in the GLME-treated
and placebo groups. In contrast, on Day 56 a higher proportion
of dogs in the GLME-treated group (28/42; 67%) showed im-
provement than in the placebo group (15/37; 41%, p=0.018).
On Day 112, when all dogs had been receiving GLME for either
56 (former placebo group) or 112 days (former GLME-treated
group), 29/32 (91%) dogs in the former placebo group and 29/37
(78%) dogs in the former GLME-treated group had improved
(p>0.05). The proportion of dogs in the former placebo group
that had improved by Day 112 (91%) was greater than the pro-
portion that had improved in that group by Day 56 (41%) on the
placebo treatment (p=0.012). In contrast, the proportion of dogs
in the GLME-treated group that improved was not signifi cantly
different (p>0.05) at Days 56 and 112.
Quantitative clinical assessment
Complete datasets for the repeated measures ANOVA were avail-
able from 70 dogs (32 from the placebo group and 38 from the
GLME-treated group). The cumulative scores from the mus-
culoskeletal examinations of both groups improved signifi cantly
from Days 0 to 28 (Figure 1). Between Days 28 and 56, cumula-
tive scores of the GLME-treated group improved signifi cantly but
those of the placebo group did not, resulting in a marginally sig-
nifi cant (p=0.053) difference between the scores of the two groups
on Day 56. Between Days 56 and 112, the cumulative scores of
both groups improved signifi cantly, and by Day 112 there was no
longer a signifi cant difference between the groups.
Tolerance
Evaluation of haematological, serum biochemical and urinalysis
data in relation to the testing laboratory’s reference ranges for each
parameter did not demonstrate any evidence of toxicity. No ad-
verse effects that were attributable to the GLME treatment were
described by the owners or the veterinarian.
Discussion
The results of this study suggest that long-term administration,
i.e. 8 weeks or longer, of GLME alleviated the clinical signs of
dogs presumptively diagnosed with mild-to-moderate DJD. The
reason for the lag period between the start of treatment with green-
lipped mussel products and clinical improvement is unknown,
but this has been reported previously (Bui and Bierer 2001).
The underlying process by which GLME has its benefi cial ef-
fects on the clinical manifestations of DJD is unknown. Extracts
of green-lipped mussel have been known for some time to have
modest anti-infl ammatory properties (Miller and Ormrod 1980;
Rainsford and Whitehouse 1980; Couch et al 1982), and the ac-
tive ingredient has variously been attributed to a proteinaceous
macromolecule (Couch et al 1982), a prostaglandin inhibitor
(Miller and Wu 1984), a glycogen extract or glycoprotein (Miller
et al 1993), or a polyunsaturated fatty acid (Whitehouse et al
1997; Halpern 2000).
The high proportion of dogs (15/47; 41%) that improved in the
placebo group during the fi rst 56 days of the trial is noteworthy
and similar to that seen in another recent trial of a nutraceutical
in dogs with arthritis (Gingerich and Strobel 2003). The present
trial was commenced in the middle of winter and most of the
recruitment into the trial was completed within 6–9 months. Ac-
cordingly, some of the improvement seen in both the GLME-
treated and placebo groups may be attributable to warmer weath-
er conditions as the trial progressed. Increased focus by owners
on appropriate rest, diet and exercise, factors already known to
infl uence the course of DJD, may also have contributed to the
improvement, as may have a ‘placebo-like effect’.
The continued improvement of the musculoskeletal scores of the
GLME-treated group during the open-label phase of the study
may have been due to the prolonged duration of administration,
which may have resulted in further clinical improvement. Alter-
natively, the perceived improvement may have been a placebo-
like effect due to the ‘unblinding’ of the owners and veterinarian.
Further research is required to establish the duration of treatment
required for optimal therapeutic effect.
Table 2. Qualitative clinical assessment of the percentage of dogs that
had or had not improved on a placebo or green-lipped mussel extract
(GLME) treatment by Day 28 and Day 56 of the placebo-controlled
phase of a trial.
Day Placebo GLME-treated
28
Improved 16 (42%) 19 (45%)
Not improved 22 (58%) 23 (55%)
56a
Improved 15 (41%) 28 (67%)
Not improved 22 (60%) 14 (33%)
a Placebo and GLME-treated groups differ signifi cantly (p=0.018)
Figure 1. Cumulative musculoskeletal examination scores of dogs
treated with either green-lipped mussel extract (GLME; ) or placebo
() for 56 days, then with GLME for another 56 days. The standard
errors (SE) for the individual datapoints were similar (0.37–0.43), and
the pooled estimate (0.39) is shown here. There was a marginally
signifi cant (p=0.053) difference between the groups at Day 56. A least
signifi cant difference (LSD) bar is shown for comparisons between
times within a group.
Cumulative clinical score
12
11
10
9
0
Days of treatment
20 60 80 100 12040
SE
LSD within
groups
117 New Zealand Veterinary Journal 54(3), 2006 Pollard et al
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A high proportion of dogs in the placebo group improved from
Day 56 (41%) to Day 112 (91%) after the placebo had been dis-
continued and replaced with open-label administration of the
GLME. This particular comparison suggests that open-label ad-
ministration of GLME to dogs with mild-to-moderate DJD is
highly likely to produce a perceived benefi cial clinical response,
but does not separate placebo effects from direct effects of the
GLME on DJD.
In conclusion, the results of this study suggest that the GLME-
containing treatment used was well tolerated and had a signifi -
cant benefi cial effect on the clinical signs of dogs presumptively
diagnosed with DJD, but that long-term therapy may be required
before improvement is apparent.
Acknowledgements
We would like to thank the staff of the Veterinary Teaching
Hospital of the Institute of Veterinary, Animal and Biomedical
Sciences, Massey University; and Estendart Ltd, for their invalu-
able nursing, technical and administrative input. The advice and
encouragement of Mr John Croft of Healtheries Ltd, Auckland,
New Zealand, is gratefully acknowledged. McFarlane Laborato-
ries NZ Ltd, Avondale, Auckland, New Zealand, provided fi nan-
cial support.
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Submitted 05 October 2005
Accepted for publication 06 March 2006
Pollard et al New Zealand Veterinary Journal 54(3), 2006 118
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