Prevalence, molecular typing and risk factor analysis for Giardia duodenalis infections in dogs in a central London rescue shelter.
ABSTRACT A cross-sectional survey to investigate canine infections with Giardia duodenalis was undertaken at a central London rescue shelter between October 2006 and March 2007. The objectives of the study were to (i) estimate the prevalence of infection in dogs admitted to a London dog shelter using a commercially available ELISA-based test kit; (ii) identify the relative importance of potential dog level risk factors for infection; and (iii) identify the occurrence of different G. duodenalis assemblages present in this population in order to identify presence of any potentially zoonotic assemblages. A faecal sample was collected from each dog entering the shelter within 1 day of arrival. Each sample was tested for the presence of parasite cyst wall protein using the Giardia SNAP test kit (Idexx Laboratories). Samples were graded for faecal consistency on a standard scale and data on age, breed, categorized breed group, sex and neutered status were collected for each dog. Associations between infection status and each dog level variable were investigated using univariable and multivariable logistic regression. Selected G. duodenalis-positive samples were genotyped using previously described primers targeting the 18S rDNA gene and the beta-giardin gene. Samples from a total of 878 dogs were collected and the true prevalence found to be 21.0% (95% CI 16.7-25.4%). In the present study, the odds of infection decreased with increasing age (adjusted odds ratio 0.66, 95% CI 0.54-0.80, p<0.0001) and was increased for Rottweilers (adjusted odds ratio 2.12, 95% CI 1.03-4.34, p=0.04). Of the 51 samples selected for genotyping, 41 samples yielded a good amplification at one or both of the targeted genes, demonstrating the occurrence of mainly dog-specific assemblages C and D. The potentially zoonotic assemblage A and a mixed template C/D were found in two individual dogs. The results of the present study illustrate the high prevalence of G. duodenalis in shelter dogs. Although predominantly infected with dog-specific assemblages, the identification of assemblage A suggests that appropriate precautions should be taken to minimize the risk of transmission to staff.
- SourceAvailable from: Antonio Varcasia[Show abstract] [Hide abstract]
ABSTRACT: The flagellate protozoan Giardia duodenalis causes infection in humans and in various animals. Eight distinct assemblages (A-H) have been identified within G. duodenalis; assemblages A and B are those specific to humans and animals, and assemblages C to H are restricted to animal hosts. The present study estimated the prevalence of G. duodenalis assemblages in dogs living in the Sardinia region and evaluated the related risk factors. Individual fecal samples were collected from 655 dogs between January 2007 and December 2010, and a form was filled out for each animal to analyze historic data that were available at the time of sampling. Fecal samples were subjected to microscopic and genetic investigations. Cysts of G. duodenalis were found in 172 (26.3%) samples, with significant values in puppies between three and nine months of age, and in kennelled and hunting dogs. The molecular characterization showed the presence of assemblages D (49%), C (36.1%), and subtype A2 (4.2%). The present survey contributes to the knowledge of the occurrence of canine giardiosis in Italy in a region with a high number of dogs and numerous animal movements, which is especially relevant for touristic reasons.The Journal of Infection in Developing Countries 05/2014; 8(5):655-60. · 1.00 Impact Factor
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ABSTRACT: To assess the potential zoonotic transmission of giardiasis from dogs in China, a total of 205 fecal specimens from dogs were screened for Giardia duodenalis using PCR and sequence analysis of the triosephosphate isomerase gene. The prevalence of G. duodenalis in dogs was 13.2% (27/205). The potentially zoonotic assemblage A and the dog-specific assemblage C was identified in 25 (12.2%) and two (1.0%) dogs, respectively. All assemblage A isolates belonged to sub-assemblage AI, genotype AI-1. Likewise, one subtype was found in assemblage C. The high occurrence of potentially zoonotic G. duodenalis subtype AI-1 in dogs that are in close contact with humans is of public health concern.Experimental Parasitology 07/2013; · 2.15 Impact Factor
- Gastroenterology 01/1995; 108(4). · 12.82 Impact Factor
Veterinary Parasitology 172 (2010) 341–346
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/vetpar
Prevalence, molecular typing and risk factor analysis for Giardia
duodenalis infections in dogs in a central London rescue shelter
Melissa Upjohna, Charlotte Cobbb, Joanne Mongerb, Thomas Geurdenc,
Edwin Claereboutc, Mark Foxb,∗
aDepartment of Veterinary Clinical Sciences, Royal Veterinary College, Hawkshead Lane, North Mymms, Hertfordshire AL9 7TA, UK
bDepartment of Pathology and Infectious Diseases, Royal Veterinary College, Royal College Street, London NW1 0TU, UK
cLaboratory for Parasitology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
a r t i c l ei n f o
Received 20 November 2009
Received in revised form 29 April 2010
Accepted 10 May 2010
a b s t r a c t
taken at a central London rescue shelter between October 2006 and March 2007. The
objectives of the study were to (i) estimate the prevalence of infection in dogs admitted
to a London dog shelter using a commercially available ELISA-based test kit; (ii) identify
the relative importance of potential dog level risk factors for infection; and (iii) identify
the occurrence of different G. duodenalis assemblages present in this population in order to
identify presence of any potentially zoonotic assemblages. A faecal sample was collected
from each dog entering the shelter within 1 day of arrival. Each sample was tested for the
presence of parasite cyst wall protein using the Giardia SNAP test kit (Idexx Laboratories).
Samples were graded for faecal consistency on a standard scale and data on age, breed,
categorized breed group, sex and neutered status were collected for each dog. Associations
between infection status and each dog level variable were investigated using univariable
and multivariable logistic regression. Selected G. duodenalis-positive samples were geno-
typed using previously described primers targeting the 18S rDNA gene and the ?-giardin
gene. Samples from a total of 878 dogs were collected and the true prevalence found to
be 21.0% (95% CI 16.7–25.4%). In the present study, the odds of infection decreased with
increasing age (adjusted odds ratio 0.66, 95% CI 0.54–0.80, p<0.0001) and was increased
for Rottweilers (adjusted odds ratio 2.12, 95% CI 1.03–4.34, p=0.04). Of the 51 samples
selected for genotyping, 41 samples yielded a good amplification at one or both of the tar-
potentially zoonotic assemblage A and a mixed template C/D were found in two individ-
ual dogs. The results of the present study illustrate the high prevalence of G. duodenalis in
shelter dogs. Although predominantly infected with dog-specific assemblages, the identifi-
cation of assemblage A suggests that appropriate precautions should be taken to minimize
the risk of transmission to staff.
© 2010 Elsevier B.V. All rights reserved.
Tel.: +44 0207 468 5225; fax: +44 0207 388 2342.
E-mail address: email@example.com (M. Fox).
ellate protozoan parasite, known to infect a wide range of
host species. In both household and kenneled dogs, infec-
tion with G. duodenalis has been described worldwide,
although the prevalence varies considerably. One of the
0304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
M. Upjohn et al. / Veterinary Parasitology 172 (2010) 341–346
reasons for such variation is the use of different diagnostic
techniques or combination of techniques, making com-
parison between these studies difficult (Claerebout et al.,
2009). The diagnosis of G. duodenalis infection is usually
based on the direct detection of cysts by faecal flotation
the past couple of years, user friendly ELISA-based tech-
niques have become available. One such test is the recently
evaluated Giardia SNAP test kit (Idexx Laboratories), which
identifies a Giardia cyst wall protein in a faecal sample and
has higher sensitivity than microscopy for epidemiological
studies (Geurden et al., 2008).
In addition to being of clinical significance in dogs,
G. duodenalis is also considered an important zoonotic
infection (Conboy, 1997). G. duodenalis comprises seven
subtypes or assemblages which have been categorized
based on genomic differences. Human isolates are typ-
ically found in assemblages A and B although other
assemblages have occasionally been reported. In canines,
the host-specific assemblages C and D are prevalent
although assemblages A and B are also frequently reported
(Thompson and Monis, 2004; Claerebout et al., 2009). The
identification of assemblages A and B suggests a poten-
tial role of dogs in zoonotic transmission and has led to
an increased awareness of the potential reservoir function
for human giardiosis (Traub et al., 2004; Lalle et al., 2005).
The most recent study investigating giardiosis in
London-based dogs was undertaken approximately 20
years ago (Sykes and Fox, 1989) and data on prevalence
and genotyping of infections in shelter animals remains
scarce. Since diagnostic technology has improved consid-
erably during the interim period, the aim of the present
study was to update knowledge on the characteristics of
G. duodenalis infection in shelter dogs in London. Specific
objectives were to (i) estimate the prevalence of infection
in dogs admitted to a London dog shelter using a commer-
importance of potential dog level risk factors for infection;
and (iii) identify the occurrence of different G. duodenalis
assemblages present in this population.
2. Materials and methods
2.1. Study design and inclusion criteria
The study was a cross-sectional survey of dogs admit-
ted to a central London rescue shelter, Battersea Dogs
Home (BDH) during the period October 2006–March 2007.
All dogs admitted to the shelter during this period were
included in the study, regardless of their signalment; as
such, it is believed that the sample is representative of the
shelter’s population during this period.
Dogs are typically presented to BDH as unwanted gifts
local government dog wardens and comprise a wide range
of breeds and ages. Dogs are drawn mainly, but not exclu-
sively, from within the London orbital road, which covers
a radius of approximately 25km from the city centre and
incorporates a mixture of urban and suburban environ-
ments. All dogs are individually housed within BDH in a
kennel with a concrete base, except for those which orig-
inated from the same household, which are housed with
one another in a single kennel.
2.2. Faecal sample collection and grading
A faecal sample was collected from the kennel of each
dog admitted within 1 day of arrival, subject to their
temperament being compatible with collection. Upon col-
lection, each sample was graded by one of two researchers
for consistency using a standard third party grading scale
of 1–5 (Zentek et al., 2004) supported by pictoral guidance,
information was also collected about each study dog and
included sex, breed, age (as assessed by trained BDH staff
using features such as teeth eruption, wear and condi-
tion and body condition criteria such as muscle mass and
prevalence of grey hairs) and neutered status (neutered vs.
2.3. Parasitological examination
tein using a commercially available ELISA (Giardia SNAP
SNAP Giardia test-positive samples collected was stored at
−20◦C prior to genotyping.
Of the 87 SNAP positive samples, 51 were selected
for genotyping, based on the availability of sufficient fae-
ces for DNA extraction. DNA was extracted using the
QIAmp Stool Mini Kit (Qiagen) according to the manufac-
turer’s instructions, incorporating an initial step of three
freeze–thaw cycles (freezing in liquid nitrogen for 5min
and heating at 95◦C for 5min) in the protocol to max-
imize cyst lysis. The eluted DNA was dissolved in 25?l
acterized using two previously described PCR protocols,
targeting the 18S rDNA gene (Wielinga and Thompson,
2007) and the ?-giardin gene (Lalle et al., 2005). Bovine
serum albumin was added to a final concentration of
0.1?g BSA/?l reaction mixture. Amplification products
were visualized on 1.5% agarose gels with ethidium bro-
mide. A positive (plasmid DNA) and negative (PCR water)
control sample was included in each PCR reaction. PCR
products were purified using the purification kit (Qiagen)
and fully sequenced using the Big Dye Terminator V3.1
Cycle sequencing Kit (Applied Biosystems) and assembled
with Seqman II (DNASTAR, Madison, WI, USA). Sequences
were compared with known sequences by BLAST analysis
against the NCBI database.
2.5. Statistical analysis
Overall prevalence and 95% confidence interval for G.
duodenalis infection were calculated; apparent prevalence
in this study was adjusted for the reported sensitivity and
M. Upjohn et al. / Veterinary Parasitology 172 (2010) 341–346
prevalence using the formula:
trueprevalence =apparentprevalence + specificity − 1
sensitivity + specificity − 1
Using those animals which returned a positive sample
as cases and all other animals as controls, a case con-
trol study was created. Data were assessed to investigate
potential signalment associated risk factors for infection
using logistical regression techniques which take account
of differences in relative representation of different cat-
egories in each variable. For analysis of association with
breed, association with each individual breed category was
assessed and association with breed grouped according to
the seven UK Kennel Club categories (Kennel Club, 2010)
was assessed separately. Univariable logistic regression
analysis was undertaken to calculate measures of strength
of association (crude odds ratios (OR)) for each indepen-
dent variable with G. duodenalis infection. For independent
variables with more than two categories, tests for linear
trend and for departure from linear trend were applied
to determine whether these variables could be modelled
in linear association with the outcome. Exposure variables
with a p-value (Wald test) of <0.20 in univariable analy-
sis were considered for inclusion in a multivariable model.
Multivariable logistic regression analysis was undertaken
to calculate adjusted odds ratios for all such variables.
A backward, stepwise removal modelling approach using
likelihood ratio tests (LRT) was employed to assess each
variable’s inclusion in the multivariable model. Variables
were retained in the multivariable model if p-values for
both the LRT and the Wald test were <0.05. All analyses
were undertaken using Stata v8.0 (Statacorp LLP, College
Station, TX) and the level of significance was set at p<0.05.
3.1. Overall prevalence
Faecal samples were collected from 878 dogs and 87
samples were found to be positive using the Idexx SNAP
test. The apparent prevalence was 9.9% (95% confidence
3.2. Faecal consistency
Of the 870 samples which were graded, 105 (11.9%)
were grade 1, 470 (53.5%) were grade 2, 216 (24.6%) were
grade 3, 57 (6.5%) were grade 4 and 22 (2.5%) were grade 5.
3.3. Dog characteristics
The majority (60.8%) of dogs participating in the sur-
vey were male. The neutered status of the majority (82.7%)
of dogs participating in the survey was entire. Whilst
42 breeds (including a category for cross breed) were
recognized, just under half (47.6%) of participating dogs
were Staffordshire Bull Terriers. The estimated age of dogs
ranged from less than 12 months to over 120 months, with
the most common age falling between 13 and 24 months
Absolute and relative frequency of different Giardia duodenalis assem-
blages, using the 18s rDNA locus (G18S) and the ?-giardin locus
2007 (n=51). NA, no amplification.
The samples analysed for genotyping spanned the
period January–March 2007. They included 10 different
breeds (including Staffordshire Bull Terriers, which com-
prised 45.6% of the subgroup) with ages ranging from 3
months to 84 months old and faecal consistency scores
between 1 and 4. The results of the genotyping are pre-
sented in Table 1. Of the 51 samples, 41 yielded good
amplification and sequencing at one or both loci. At the
18s rDNA locus, 36 samples yielded a good amplification
whereas only 15 had a good amplification using the ?-
giardin locus. Of the 15 ?-giardin positive samples, 10
also yielded a positive amplification with the 18s rDNA
primers. In general, the genotyping results demonstrated
the occurrence of mainly the dog-specific assemblages C
and D in the BDH dogs, although in one dog the potentially
zoonotic A3 subgenotype was found using the ?-giardin
gene. In one sample, a mixed template containing assem-
blage C (on the 18S rDNA gene) and assemblage D (on
the ?-giardin gene) was found. The sequence for the ?-
giardin locus are available at Genbank under Genbank
accession numbers HM061150–53, and the sequences for
the 19s rDNAa locus under Genbank accession numbers
3.5. Statistical analyses of association
Univariable logistic regression of infection status with
respect to dog level variables showed the results set out
in Table 2. On the basis of univariable analysis, there was
evidence of association between neutered status (being
entire), age (the younger the age group, the greater the
odds of infection) and breed (being a Rottweiler) and being
infected with G. duodenalis. There was no evidence to sup-
port an association between G. duodenalis infection and
either sex, faecal consistency or Kennel Club breed group.
respect to those dog level variables which met the pre-
defined inclusion criteria resulted in a final model which
comprised two variables as set out in Table 3. Age (younger
age group) and breed (being a Rottweiler) remained signif-
icantly associated with increased odds of infection in the
multivariable model, whereas neutered status did not.
M. Upjohn et al. / Veterinary Parasitology 172 (2010) 341–346
Univariable logistic regression analysis of Giardia duodenalis infection with respect to dog level variables investigating associations between G. duodenalis
infection and sex, age, neutered status, faecal consistency and breed of dog sampled at Battersea Dogs’ Home October 2006–March 2007 (n=878 for sex
and neutered status; n=851 for age; n=870 for faecal consistency). SBT, Staffordshire Bull Terrier; PWaldvalue, p-value for Wald test.
Each incremental older category
Each incremental grade
1.11 790.86 1.44 0.433
Multivariable logistic regression analysis of Giardia duodenalis infection with respect to dog level variables showing associations between G. duodenalis
infection and age and breed of dog sampled at Battersea Dogs’ Home October 2006–March 2007 (n=851 for age; n=878 for breed). SBT, Staffordshire Bull
Terrier; PWaldvalue, p-value for Wald test; PLRTvalue, p-value for likelihood ratio test.
Variable CategoryCases, n
Adjusted odds ratio
PLRTvalue 95% confidence interval
Each incremental older category
There have been many previously published studies of
G. duodenalis prevalence in dog populations. These previ-
ous studies covered a wide range of population settings
(urban or rural), income (both developing and developed
hospitalized, owned or stray), health status and variable
age ranges. This variability in population characteristics, as
well as variation in the diagnostic methodology applied in
different studies, makes direct comparisons between stud-
ies difficult. Data relating to stray dog populations and, in
particular, on genotyping for this sub-population remains
The apparent prevalence recorded in this study (9.9%)
was lower than that described in the most directly compa-
rable study (in terms of location) reported approximately
20 years ago (Sykes and Fox, 1989) which was an appar-
ent prevalence of 14.5%. Since validated sensitivity and
specificity values for the ELISA are available, it was pos-
sible to calculate a true prevalence of infection for this
study (21.0%) but in the absence of such values for the
original test methodology direct comparison of the true
prevalence is not possible. The prevalence recorded in
the present study lies within the prevalence range (<1%
to 45%) reported in other shelter based studies in Brazil,
Italy, Spain, Belgium and the Czech Republic (Huber et al.,
2005; Papini et al., 2005; Dubna et al., 2007; Martinez-
Carrasco et al., 2007; Meireles et al., 2008; Claerebout et
ever, the same SNAP test was used as in the present study
(Carlin et al., 2006) and a comparable overall prevalence of
between individual states participating in the investiga-
The increased risk associated with younger animals in
the current study concurs with findings reported by other
studies (Sykes and Fox, 1989; Jacobs et al., 2001; Papini
et al., 2005; Claerebout et al., 2009). However, it contra-
dicts the findings reported by Haralabidis et al. (1988) in
Greece (overall prevalence of 0.8%) which found no asso-
ciation with age although the lack of association in the
latter study might be due to the low prevalence. Over half
of the samples were recorded as grade 2 (described as
“well formed”; Zentek et al., 2004). The lack of association
between faecal consistency and infection in this study con-
firms previously reported findings (Winsland et al., 1989;
Jacobs et al., 2001; Oliveira-Sequeira et al., 2002; Itoh et al.,
2005; Papini et al., 2005). The uncertainty surrounding this
rhoea was believed to be a reliable clinical sign of infection
(especially in humans). Based on the findings in this study,
clinicians may be under-diagnosing infection in practice if
they are relying on (reported) diarrhoea as an indication of
the need to screen for G. duodenalis.
prised almost half the total number of dogs represented
in this study, the large number of breeds recorded in the
study indicates the mixed nature of London’s pet dog pop-
ulation. The increased risk associated with Rottweilers in
this study was unexpected and may be worthy of further
M. Upjohn et al. / Veterinary Parasitology 172 (2010) 341–346
In 41 of the 51 samples on which genotyping was
undertaken, the parasite assemblage was identified. The
difference in PCR sensitivity between the 18S rDNA locus
and other loci has been described previously (Leonhard
et al., 2007) and is expected, since it is a mitochondrial
gene and is therefore present in multiple copies through-
are single copy genes. The G. duodenalis genotyping in
the present study with predominately the dog-specific
assemblages C and D confirms previous findings (Berrilli
et al., 2004; Zygner et al., 2006; Szenasi et al., 2007;
Claerebout et al., 2009). It was suggested by Thompson
and Monis (2004) that there may be two cycles of trans-
mission taking place in dogs. Transmission of dog-specific
isolates may be favoured by intensive contact between
large numbers of dogs living together, such as in shelters.
Under these circumstances, the dog-adapted genotypes
may out-compete other genotypes. In household dogs, the
frequency of dog to dog transmission will be less and
thus infections acquired with assemblage A genotypes in
dogs are likely to persist. This hypothesis is, however, only
partially supported by studies reporting a high percent-
age of assemblage A in household dogs (Lalle et al., 2005;
Leonhard et al., 2007; Claerebout et al., 2009) and high per-
centages of assemblages C and D in kennel dogs (Berrilli
et al., 2004; Szenasi et al., 2007) whereas in other surveys
household dogs were mainly infected with assemblages C
and D (Itagaki et al., 2005; Rimhanen-Finne et al., 2007;
Overgaauw et al., 2009) and kennel dogs harboured pre-
dominately assemblage A (Itagaki et al., 2005; Leonhard et
The results of the present study reveal a high preva-
lence of G. duodenalis in dogs entering the BDH shelter and
a predominance of the dog-specific assemblages C and D.
Although in the present study only one dog was found to
is still appropriate as mixed infections with both the dog-
specific and zoonotic assemblages cannot be ruled out by
the genotyping techniques used in the present study. It is
therefore important that those working with such animals
– including veterinary workers, kennel staff and shelter
priate precautions to prevent infection.
The authors wish to acknowledge the generous supply
of Giardia SNAP Test kits by Idexx Laboratories, access to
dog faecal samples and associated background informa-
tion at Battersea Dogs’ Home and funding by The Royal
Veterinary College (University of London).
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