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R E S E A R C H Open Access
Cross-reactions of sera from dogs infected with
Angiostrongylus vasorum in commercially
available Dirofilaria immitis test kits
Manuela Schnyder
*
and Peter Deplazes
Abstract
Background: Dirofilaria immitis and Angiostrongylus vasorum are both important potentially fatal canine nematodes
with overlapping endemic areas, especially in Europe. The preadult and adult stages of both species are living in
the Arteria pulmonalis and the right heart, and diagnostically detectable circulating parasite antigens have been
demonstrated for both species. For the detection of D. immitis infections, a variety of commercial tests have been
developed, however, they have not been evaluated for cross-reactions against circulating antigens of A. vasorum.
Methods: In this study, potential cross-reactions of sera from 16 dogs, which were experimentally infected with A.
vasorum and which had circulating antigens as confirmed by a species-specific ELISA, were evaluated for the
detection of A. vasorum antigen in six commercially available D. immitis test kits.
Results: In three fast tests (Witness
W
Dirofilaria, SensPERT
W
Canine Heartworm, SNAP
W
4Dx
W
Plus), all sera were
negative. One fast membrane ELISA (SNAP
W
HTWM RT Test) was positive with four sera (25%), and one serum
delivered a non-valid result twice. In the PetChek
W
HTWM PF Test, depending on the interpretation protocol, 5 or 8
dogs (31.2 –50%) were positive. With the DiroCHEK
W
-ELISA, a single A. vasorum-infected dog (6.2%) tested positive.
Conclusions: Due to potential cross-reactions with A. vasorum in commercially available test kits for the detection
of D. immitis antigen, the simultaneous use of highly specific diagnostic methods for the differentiation of these
two canine heart worms is recommended.
Keywords: Angiostrongylus vasorum,Dirofilaria immitis, Antigen detection, Cross-reactions, Dogs
Background
The adult stages of Dirofilaria immitis, a filarial nema-
tode, and Angiostrongylus vasorum, a metastrongylid
nematode, are both localized in the Arteria pulmonalis
and the right heart of their definitive hosts. Dogs, foxes
and some other carnivores are the definitive hosts of
both parasites, while Culicidae and Gastropoda are the
intermediate hosts of D. immitis and A. vasorum,
respectively.
In Europe, D. immitis is present in coastal Mediterra-
nean areas with expansion northwards, while in North
America the parasite has expanded from the south-
eastern coastal areas northwards and westwards [1] up
to Canada [2]. A. vasorum was diagnosed for the first
time in France in 1913 [3], but it is only recently that
this parasite has regained attention within the veterinary
community [4,5]. Its presence has been increasingly
reported from several new areas in and outside Europe
(reviewed in [6]). Reports of an increasing number of
cases of canine angiostrongylosis, as well as the develop-
ment of new diagnostic tools such as ELISAs [7-10] or
biomolecular techniques [11,12] may have contributed
and also incentivised epidemiological studies, confirming
the presence of this parasite in dogs, foxes and snails
throughout Europe. The Atlantic provinces of New-
foundland and Labrador are the only regions actually
affected by A. vasorum in North America, with a poten-
tial for expansion to further regions [4,13,14]. Overlap-
ping areas in large parts of southern Europe with the
presence of both A. vasorum and D. immitis have there-
fore to be accounted for. Furthermore, in non-endemic
* Correspondence: manuela.schnyder@uzh.ch
Institute of Parasitology, Vetsuisse Faculty, Winterthurerstrasse 266a, 8057,
Zürich, Switzerland
© 2012 Schnyder and Deplazes; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the
Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
Schnyder and Deplazes Parasites & Vectors 2012, 5:258
http://www.parasitesandvectors.com/content/5/1/258
areas of D. immitis, this agent has to be considered
based on anamnestic information (travelling with pet
dogs or imports) and differentiated from A. vasorum
infections.
Fatal clinical consequences of D. immitis infection are
usually prevented by the monthly use of macrocyclic lac-
tones in known endemic areas [15-17], and treatment of
dirofilariosis is based on the intramuscular application of
the arsenic derivate melarsomine [18] and/or, alterna-
tively, by eliminating the endosymbiont Wolbachia with
doxycycline supported by administration of macrocyclic
lactones [19]. Dogs infected with A. vasorum, instead,
are treated using macrocyclic lactones such as moxidec-
tin [20] or milbemycin-oxime [13], or applying fenben-
dazole [21]. Prophylactic treatment (with macrocyclic
lactones) against potentially fatal canine angiostrongylo-
sis is, as for dirofilariosis, recommended in highly en-
demic and well known areas [20].
The currently used diagnostic laboratory methods for
the detection of these parasites are divergent. The diag-
nosis of D. immitis is based on the detection of microfil-
ariae or circulating antigens released by mature adult
female worms into the blood circulation, both being de-
tectable starting from 6 months after infection [18]. A
variety of tests have been developed for the detection of
circulating antigens, employing lateral flow immuno-
chromatographic techniques, membrane ELISAs or con-
ventional ELISAs [22-24]. Test evaluations showed that
the sensitivity of heartworm antigen tests depends on
the worm burden, and the sex and age of the parasites
[24-28], while the specificity of the kits is regularly indi-
cated to be very high, between 95% and 100%
[23,25,26,29,30]. However, only occasionally were poten-
tial cross-reactions evaluated in animals with natural or
experimental infections with other helminths, mainly
against other filarial nematodes such as Dipetalonema
reconditum [22,31] or Dirofilaria repens, indicating that
modern test kits may overcome cross-reactions detected
in previously developed test kits for these parasites
[32,33], and, rarely, against intestinal parasites such as
Ancylostoma caninum and Trichuris spp. [22,34]. The
most current diagnostic method for detection of A.
vasorum infections in dogs is the isolation of first stage
larvae (L1) from faecal samples, which are produced by
the parasites approximately 6–7 weeks after infection.
Larval migration techniques such as the Baermann-
Wetzel method [35] are commonly adopted. Further-
more, ELISAs for the detection of antibodies against A.
vasorum have been described [7,9], and, recently, tests
for the detection of circulating antigen of A. vasorum
have been developed. These latter ones have been evalu-
ated for cross-reactions against Crenosoma vulpis [8,10]
and also against intestinal parasites (Toxocara canis,
Ancylostoma caninum) and, importantly, against D.
immitis [8], showing a high specificity (94-100%).
Due to their common localization within the definitive
hosts, their considerable size and particularly the well
documented production of circulating antigens [31,36],
it was argued that antigens of A. vasorum and D. immitis
may share epitopes responsible for potential cross-
reactions in antigen detection tests. This hypothesis has
been confirmed during the development of the ELISA
for the detection of circulating antigen for A. vasorum
[8].
The aim of the study was to evaluate potential cross-
reactions of sera from dogs experimentally infected with
A. vasorum in six different commercially available tests
for the detection of D. immitis antigen.
Methods
A total of 16 sera from dogs experimentally inocu-
lated with 200 third stage larvae (L3) of A. vasorum
were obtained during previously performed studies
[20,37]. Infection of dogs was confirmed by positive
Baermann-Wetzel analyses [35], by the detection of
circulating A. vasorum antigen [8] and by the pres-
ence of adult worms at necropsy adopting an estab-
lished method of reverse lung perfusion [20]. The
day of sample collection (between 55 and 356, mean
101) after inoculation (dpi) and the number of
detected parasites at necropsy are shown in Table 1.
Worm burdens varied between 10 and 170 adult parasites,
with a mean of 66 worms per dog. Dirofilaria immitis
infection was excluded based on the fact that the dogs
were living in a non-endemic area under controlled ex-
perimental conditions, and at necropsy.
All tests were performed blinded with an identity
code from 1 to 16, by veterinarians (fast tests) or by
experienced laboratory technicians from the IPZ
(ELISAs).
All sera were non-haemolytic, stored at −20°C and
tested within 11–40 months after collection. The follow-
ing test kits were used, adopting the manufacturer’s in-
struction and within the indicated expiry dates:
1) Witness
W
Dirofilaria, lateral flow (Synbiotics, San
Diego, USA)
2) SensPERT
W
Canine Heartworm, lateral flow (VetAll
Laboratories, Kyunggi-Do, South Korea)
3) SNAP
W
HTWM RT, membrane ELISA (IDEXX
Laboratories, Westbrook, USA)
4) SNAP
W
4Dx
W
Plus, membrane ELISA (IDEXX
Laboratories, Westbrook, USA)
5) Petchek
W
HTWM PF Antigen Test , ELISA (IDEXX,
Westbrook, USA)
6) DiroCHEK
W
, ELISA (Synbiotics San Diego, USA)
Schnyder and Deplazes Parasites & Vectors 2012, 5:258 Page 2 of 5
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Results
Single test results are shown in Table 1. All tests, with
one exception (see Tab. 1, dog Av 8) fulfilled the criteria
for test validity based on the results of positive and/or
negative controls.
The ELISA for the detection of circulating A. vasorum
antigen was highly positive for all experimentally
infected dogs, with absorbance values (optical density
read at 405 nm, OD) varying between 0.263 and 2.007
(cut-off value: 0.159, as previously described [8]), with a
mean of 1.096.
In three fast tests (Witness
W
, SensPERT
W
,SNAP
W
4Dx
W
Plus) all sera resulted negative, while in one fast
membrane ELISA (SNAP
W
HTWM RT) four A. vasorum
infected dogs were positive for D. immitis antigen, and
one serum delivered a non-valid result twice. In the
PetChek
W
-ELISA two methods for interpretation were
adopted: following the instruction for veterinary practi-
tioners based on eye detection, 5 dogs resulted positive
for D. immitis infection, while following the instructions
under laboratory conditions with OD measurements, a
total of 8 dogs were seropositive. With the DiroCHEK
W
-
ELISA, a single A. vasorum infected dog was D. immitis
seropositive. With one exception (76 dpi), all cross-
reactions were observed in dogs infected with A.
vasorum for more than 90 days, with worm burdens
varying from 10–170.
Discussion
This study provides evidence of false positive reactions
in D. immitis antigen detection kits with sera of dogs
infected with A. vasorum. The two ELISAs for D. immi-
tis detection (PetChek
W
and DiroCHEK
W
) and the mem-
brane ELISA SNAP
W
HTWM RT showed single cross-
reactions against A. vasorum, which had not been con-
sidered so far. In contrast, the adopted ELISA for the de-
tection of circulating A. vasorum antigen has been
developed evaluating different monoclonal antibodies,
which had been selectively chosen based on their ab-
sence of cross-reactivity against D. immitis circulating
antigens, resulting in an overall high specificity [8].
Table 1 Comparative results of 16 sera from dogs experimentally inoculated with Angiostrongylus vasorum (Av) tested
with 6 different diagnostic kits for the detection of D. immitis antigen and with an ELISA for detection of A. vasorum
circulating antigen [8]
Dog-ID Days post
inoculation
(dpi)
Worm
burden
(n)
A. vasorum
antigen detection
(optical density)
1
Diagnostic test kits for the detection of Dirofilaria immitis antigen
Witness
W
SensPERT
W
SNAP
W
HTWM RT
2
SNAP
W
4Dx
W
Plus
PetChek
W
(veterinary
practice
conditions)
3
PetChek
W
(laboratory
conditions)
3
DiroCHEK
W
Av 1 55 49 1.484 neg. neg. neg. neg. neg. neg. neg.
Av 2 55 54 1.825 neg. neg. neg. neg. neg. neg. neg.
Av 3 55 106 1.743 neg. neg. neg. neg. neg. neg. neg.
Av 4 55 129 1.400 neg. neg. neg. neg. neg. neg. neg.
Av 5 55 134 1.485 neg. neg. neg. neg. neg. pos. neg.
Av 6 59 57 0.567 neg. neg. neg. neg. neg. neg. neg.
Av 7 59 98 0.657 neg. neg. neg. neg. neg. neg. neg.
Av 8 76 32 0.263 neg. neg. not valid neg. low pos. pos. pos.
Av 9 76 42 0.520 neg. neg. neg. neg. neg. neg. neg.
Av 10 76 68 1.007 neg. neg. neg. neg. neg. pos. neg.
Av 11 90 13 0.879 neg. neg. neg. neg. neg. pos. neg.
Av 12 90 30 1.069 neg. neg. neg. neg. neg. neg. neg.
Av 13
4
91 10 1.264 neg. neg. low pos. neg. low pos. pos. neg.
Av 14
4
91 170 1.396 neg. neg. low pos. neg. low pos. pos. neg.
Av 15 286 36 2.007 neg. neg. low pos. neg. pos. pos. neg.
Av 16 356 24 1.357 neg. neg. low pos. neg. pos. pos. neg.
1
: optical density values read at 405 nm.
2
: SNAP
W
HTWM RT test differentiates between low positive (low pos.) and positive results.
3
: The interpretation of PetChek
W
results can be done under an “In-clinic”-protocol based on subjective colour evaluation or under the “Laboratory protocol”by
measuring the optical densities at 650 nm and a cut-off calculation based on positive and negative controls.
4
: dog Av 13 and Av 14 were inoculated with 50 and 500 L3, respectively.
neg.: negative.
pos.: positive.
Schnyder and Deplazes Parasites & Vectors 2012, 5:258 Page 3 of 5
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Generally, D. immitis antigen tests are considered to
be more sensitive than microfilariae concentration meth-
ods or other procedures [38]. In particular, the ELISA
technology has been shown to be more sensitive than
lateral flow immunochromatography [26] for the diagno-
sis of heartworm infected dogs. Reasons for the occur-
rence of false negative results with sera of D. immitis –
positive dogs have been discussed in previously per-
formed studies evaluating different D. immitis test kits.
Low worm burden and low number of female worms
have been shown to reduce sensitivity of the tests
[25,26,39]. However, increased sensitivity may be
coupled with lower specificity and, importantly, with po-
tential cross-reactions against A. vasorum. An unknown
number of dogs with travel anamnesis and testing posi-
tive for circulating heartworm antigen may have falsely
been diagnosed positive due to A. vasorum cross-reac-
tions, and erroneously treated with melarsomine and/or
macrocyclic lactones. Therefore, serological results for
D. immitis should be confirmed or excluded by add-
itional diagnostic tests (Knott’s test for microfilariae of
D. immitis, or serology or Baermann migration test for
L1 of A. vasorum) or diagnostic imaging frequently deli-
vering pathognomonic findings for heart dirofilariosis
[40,41] or angiostrongylosis [42,43].
Conclusions
In this study we confirmed that sera of dogs infected
with A. vasorum cross-react in commercially available
test kits for the detection of circulating D. immitis anti-
gen. The simultaneous use of highly specific diagnostic
tools is recommended for epidemiological studies where
both heart worm species occur or for individual dogs
with a suspected heart worm infection.
Competing interests
The authors declare that they have no competing interests.
Authors’contributions
MS participated in the design of the study, collected the samples, carried out
the diagnostic assays and drafted the manuscript. PD conceived the study
and implemented the draft of the manuscript. Both authors have read and
approved the final manuscript.
Acknowledgements
Authors sincerely thank Christine Sperlich and Vera Kaspar for technical
assistance, Dr. Jeongmi Kim (VetAll Laboratories, Korea) for the free provision
of the test kits and IDEXX Laboratories for providing of SNAP
W
4Dx
W
Plus
test kits.
Received: 26 September 2012 Accepted: 8 November 2012
Published: 13 November 2012
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doi:10.1186/1756-3305-5-258
Cite this article as: Schnyder and Deplazes: Cross-reactions of sera from
dogs infected with Angiostrongylus vasorum in commercially available
Dirofilaria immitis test kits. Parasites & Vectors 2012 5:258.
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