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Veterinary Dermatology 2002, 13, 39 44

BlackwellArticle
Original
Science, Ltd

Sensitivity patterns to house dust mites and forage mites in

atopic dogs: 150 cases
EMMANUEL BENSIGNOR* and DIDIER N. CARLOTTI
**Dermatology Referral Service, Veterinary Clinic, 17 bvd des Filles du Calvaire, 75003 Paris, France
Cabinet de Dermatologie Vtrinaire, avenue de Magudas, 33700 Bordeaux-Mrignac, France
(Received 12 February 2001; accepted 28 June 2001)

Abstract This study investigated intradermal test reactions to extracts of six species of mites in 150 dogs with
atopic dermatitis. At least one positive reaction was seen in 120 animals (80%). Dermatophagoides farinae
attracted the highest number of positive reactions (108 dogs, 90% of dogs and 72% of atopic dogs showing positive
reactions). Positive reactions to other mites were not uncommon, with many dogs testing positive for Dermatophagoides pteronyssinus (32% of dogs tested), Acarus siro (35%), Tyrophagus putrescentiae (30%), Glycyphagus
domesticus (27%) and Lepidoglyphus destructor (23%). Sensitivity to D. farinae alone occurred commonly (57%
of cases), but multiple sensitivities were seen frequently with the other mites. Cases of sensitivity to only one mite
were also seen: D. pteronyssinus (five cases), T. putrescentiae (one case) and G. domesticus (one case). Further studies are needed to appreciate more clearly the precise role played by the different species of mite in canine atopic
dermatitis.
Keywords: allergy, atopic dermatitis, intradermal test reactions, mites.

INTRODUCTION
Atopic dermatitis is a complex syndrome, the aetiopathogenesis of which is still poorly understood.1
Various causal factors have been identified. In man,
genetic abnormalities, impaired barrier function of
the epidermis (in particular the stratum corneum),
immune system disorders and abnormal reactions to
common environmental substances (aeroallergens,
foods and perhaps even haptens) have been suggested.1,2 The situation is the same in the dog.35 The
role played by bacterial, fungal and psychological
factors is important but is still poorly understood in
both species.15 Although the extent to which allergic
mechanisms are involved in the pathogenesis of this
dermatosis is disputed,2 most authors agree that it is
considerable. In this context, mites are strongly suspected of being involved in provoking and/or exacerbating lesions of atopic dermatitis, in both man and
dogs.19 This is corroborated by positive allergy tests,
and by the good response to avoidance measures in
man10 and specific desensitization in the dog.
In the human allergy field, forage mites, as well as
pyroglyphid mites, have been shown to play an important role in the development of allergic asthma.11 Studies have also been carried out to investigate the most
common sensitivities in atopic dogs.4,6,7 It is now well
known that D. farinae is the most common source of
allergens commonly provoking positive reactions in
Correspondence: E. Bensignor, Dermatology Referral Service,
Veterinary Clinic, 17 bvd des Filles du Calvaire, 75003 Paris, France.
E-mail: emmanuel.bensignor@wanadoo.fr
2002 Blackwell Science Ltd

dogs in Europe, whereas D. pteronyssinus is the main

source of allergen involved in human asthma. Few
studies, however, have reported sensitivities to the various other different species of mite in atopic dogs.12 14
In this prospective study, intradermal testing was
used to investigate sensitivity patterns in 150 atopic
dogs to six mites found in our environment15 (two
Pyroglyphidae, D. farinae and D. pteronyssinus, two
Acaridae, Acarus siro and Tyrophagus putrescentiae
and two Glycyphagidae, Glycyphagus domesticus and
Lepidoglyphus destructor).

MATERIALS AND METHODS

Animal selection
We recruited 150 dogs of various breeds. The animals
had all been referred to a veterinary dermatologist in
Aquitaine, France, over a period of 2 years.
Diagnosis of atopic dermatitis
For each animal, atopic dermatitis was diagnosed from
the conjunction of epidemiological and clinical data
and immunological criteria (demonstration of type 1
hypersensitivity by the presence of at least one positive
reaction within 20 min of an intradermal test). Clinical
diagnosis was based on criteria proposed by Willemse
(Table 1),16 to which the presence of erythematoceruminous otitis and erythematous pododermatitis
were added as major criteria, as suggested by Prlaud
et al. 17
In each case, the possibility of ectoparasitic infestation was excluded by microscopic examination of skin
39

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40

E. Bensignor and D. N. Carlotti

Major criteria (at least three)

Minor criteria (at least three)

Pruritus
Appearance and distribution of lesions:
face and /or limbs
lichenification of the hock and /or cranial carpus
chronic dermatitis
Predisposed breed or familial history

Age of onset between 1 and 3 years

Facial erythema
Conjunctivitis
Superficial pyoderma
Hyperhidrosis
Positive intradermal reactions elevated
Allergen-specific IgGd
Elevated allergen-specific IgE

scrapings, and trial acaricidal therapy where appropriate (ivermectin; Ivomec, 0.300 mg kg1 SC twice
at a 14-day interval). Rigorous flea control was also
systematically undertaken for every case (using an
adulticide and insect growth regulator).
Whenever bacterial pyoderma and/or Malassezia
dermatitis were present (diagnosed by clinical examination and cytology), animals were given specific treatment (antibiotics; cefalexin, Rilexine, 30 mg kg1
orally twice daily and/or systemic antifungals; ketoconazole, Ketofungol, 10 mg kg1 orally once daily) in
association with a twice weekly application of a 3%
chlorhexidine shampoo for 3 weeks prior to being
included in the study. Only animals that were still pruritic, and had lesions compatible with atopic dermatitis
after resolution of infection, were recruited.
All animals were fed a restricted diet consisting of
novel proteins (horse meat or fish) and one source of
vegetables (potatoes or semolina), for between 4 and
8 weeks (on average 6 weeks).18 Only animals showing
no marked reduction in pruritus and skin lesions after
this food trial were recruited.18
In every case, drugs were withheld prior to intradermal testing in accordance with recommendations
in the literature (antihistamines 1 week, oral corticosteroids 3 weeks, injectable corticosteroids 16 months).18
Intradermal tests
The test allergens were house dust mites or forage mites,
commonly identified as causal agents in both animal
and human allergy. Extracts of D. farinae, D. pteronyssinus,
T. putrescentiae, A. siro, G. domesticus and L. destructor
were used. These extracts were used in concentrations
previously demonstrated not to be irritant (1000 UI mL1
for D. farinae and D. pteronyssinus, 0.1% for other mites),
by the absence of positive reaction after challenging
10 healthy dogs (privately owned dogs not suffering
from any disease). These extracts were supplied by
Isotec Laboratories (BP 220-10 av. Ampre, F-78051,
St Quentin en Yvelines, France). In order to validate
reactions to the other extracts, two controls were also
used: a positive control (histamine phosphate 0.01%)
and a negative control (phenolated physiologic diluent).
Intradermal tests were conducted in accordance
with standard protocols,18 if necessary for nervous
animals under general anaesthetic, previously demonstrated not to interfere with intradermal testing in
dogs (atropine/tiletamine/zolazepam).18 Animals were
clipped carefully over the thorax, and injection sites
marked with indelible ink. Each allergen (0.05 mL) was
2002 Blackwell Science Ltd, Veterinary Dermatology, 13, 39 44

Table 1. Willemses diagnostic criteria for

atopic dermatitis16

injected intradermally using an insulin syringe and

sterile needle. Reactions were read after 1520 min, in
darkness, under a source of oblique light. The diameter
of every reaction was measured precisely with a small
ruler supplied by the allergen company.18
Reactions were assessed according to criteria validated
in previous studies in the dog;18 briefly, for a reaction to
be considered positive, an oedematous, erythematous
plaque, larger in diameter than that of the average of
the positive and negative controls, had to be present.18
In the absence of erythema, or if reactions were of inadequate diameter, reactions were considered negative.

RESULTS
Epidemiological data
One hundred and fifty dogs, of various ages (average
3.8 years) and breeds, were included in the study. No
sex predilection was observed. No breed predilection
could be determined because of the lack of a reference
population.
Interpretation of skin tests
Interpretation of the skin test was possible in all cases.
No adverse reactions associated with the skin tests
were seen. No difference in reactions was seen in the
anaesthetized vs. nonanaesthetized dogs.
Positive reactions to at least one of the mites tested
were seen in 120 animals (80% of cases). No positive reactions to any mite were seen in 30 animals (20%). Results
of all positive intradermal tests are shown in Fig. 1.
Dermatophagoides farinae was the species of mite
eliciting the highest number of positive reactions: 108
dogs (72% of atopic dogs and 90% of positive dogs)

Figure 1. Frequency distribution of intradermal test results in the

120 dogs showing positive reactions.

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Mite sensitization in canine atopic dermatitis

showed a positive reaction to this mite. A positive reaction to D. pteronyssinus was seen in only 38 animals
(25% of atopic dogs and 32% of dogs testing positive).
Of all the dogs testing positive, 64 (54%) were sensitive exclusively to D. farinae and/or D. pteronyssinus, with
no positive reactions to the four other species of mite.
In 69 dogs (57%), a positive reaction was seen for
D. farinae and not for D. pteronyssinus. Conversely,
in five cases (3%), a positive reaction was seen to
D. pteronyssinus and not to D. farinae. In 33 dogs
(27%), a positive reaction was seen to both D. pteronyssinus and D. farinae.
Positive reactions to other species of mite were
observed in 56 animals (46% of cases) and occurred as
follows: A. siro (42 cases, 28% of all dogs tested and
35% of dogs testing positive) and other forage mites
(56 cases, 37% of all dogs tested and 46% of dogs
testing positive). Among these other forage mites were
T. putrescentiae (36 cases, 24% of all dogs tested and
30% of dogs testing positive), G. domesticus (32 cases,
21% of all dogs tested and 27% of dogs testing positive)
and L. destructor (28 cases, 19% of all dogs tested and
23% of dogs testing positive) (Table 2).
In most cases, sensitivities to more than one mite
were seen (Fig. 2). A positive reaction to either
Table 2. number and percentage of dogs showing positive reactions
to forage mites
Source(s) of
positive reactions

Number of
positive cases

Percentage (%)

T
A
L
G
T and A
L and A
L and G
T and L
T, A and L
T, A and G
A, L and G
T, A, L and G

5
3
0
1
13
3
1
2
6
1
6
15

9
5
0
2
23
5
2
4
11
2
11
26

T, Tyrophagus putrescentiae; A, Acarus siro; L, Lepidoglyphus

destructor; G, Glycyphagus domesticus.

Figure 2. Percentage of dogs showing 1, 2, 3 and 4 positive reactions

to forage mites.

41

Table 3. Sensitivity patterns in dogs where positive reactions were

seen exclusively to forage mites
Source(s) of
positive reactions

Number of
positive cases

Percentage (%)

T
G
T and A
T and L
T, L and A
A, L and G
A, L, G and T

1
1
1
1
1
1
2

12.5
12.5
12.5
12.5
12.5
12.5
25

T, Tyrophagus putrescentiae; A, Acarus siro; L, Lepidoglyphus

destructor; G, Glycyphagus domesticus.

D. farinae or D. pteronyssinus was often associated

with positive reactions to other species of mite: of
56 animals with positive reactions to A. siro,
T. putrescentiae, L. destructor and/or G. domesticus,
only eight cases were positive solely to forage mites.
Exclusive sensitivity to A. siro was not seen. The
incidence of positive reactions is shown in Table 3.
Of these, reactions to T. putrescentiae were the most
common, being positive in six of eight animals (75%),
compared with four for G. domesticus (50%), and five
for A. siro and L. destructor (62.5%).

DISCUSSION
This study increases our understanding of house
dust mite and forage mite sensitivity in atopic dogs.
Sensitivity to these sources of allergens was extremely
common in our sample of atopic dogs. Eighty per cent
of animals tested showed at least one positive reaction
to one of these mites. This finding is in line with data in
the French literature,4,6,7 and confirms the importance
of mite sensitivity (house dust and forage) in canine
atopic dermatitis (CAD). The high incidence of positive reactions to mites in atopic dogs can probably be
explained in part by the conditions in which pet animals are kept (for example, humid flats, excessive heating, bedding).
The importance of the pyroglyphid mite, D. farinae,
was also, as expected, reaffirmed.4 7,19 This was the
source of allergens most frequently giving positive
reactions (almost 75% of cases). Ninety per cent of
dogs with positive reactions to mites were sensitive to
D. farinae. Other species were involved a lot less frequently. It is worth noting, however, that positive reactions to these other mite species were seen in over a
quarter of CAD cases, which is far from negligible.
These data are different from those published in
human allergology, in which D. pteronyssinus is the
main allergen in asthmatic patients.1,2 This difference
has not yet been explained, but may be linked to variations in epitopes between the different species of
mites, and/or between major allergens in man and dog,
as already demonstrated for D. farinae.20
Sensitivity to D. farinae alone occurred commonly,
in 62% of cases. Sensitivity to D. pteronyssinus alone
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42

E. Bensignor and D. N. Carlotti

was much less common (five cases, 4%), as observed

previously in France,4,6,7 but not in a Danish study
reported in conference proceedings by F. Kristensen
(Proceedings of the First FECAVA-CNVSPA Congress, Paris, 1994, pp. 7558). With the other mites,
multiple sensitivity seems to be the rule. Multiple
sensitivity was varied and it was not possible to determine preferred cross-reactions between these species.
Sensitivity to a forage mite alone was also seen (two
cases) and there were cases for which only forage
mites were positive (no reactions to D. farinae and
D. pteronyssinus) (eight cases). These instances of
single sensitivity suggest, as has been found in man,11
that cross-reactions do not occur systematically between
forage mites tested in the dog. If the intradermal test
reagents did systematically cross-react, it would be reasonable to assume that there would always be positive
reactions to several mites, and that single sensitivities
would not occur. However, from our data, conclusions
cannot be made regarding possible allergen crossreactivity in any one individual. In man, studies have
either not identified cross-reactions between D. farinae
or D. pteronyssinus and the forage mites21,22,23 either
found a cross-reactivity by RAST inhibition techniques.24 Forage mites and pyroglyphids mites are very
different species, and the absence of systematic crossreactions is therefore not surprising.25
The high incidence of reactions to various species of
mite in this study is also interesting from the therapeutic standpoint. First, specific allergens responsible
for the allergy, or thought to be responsible, should be
included in any desensitization protocol. A recent study
(F. Kristensen, Proceedings of the First FECAVACNVSPA Congress, Paris, 1994; pp. 7558). compared
the efficacy of desensitization to D. farinae and D.
pteronyssinus in the dog, using either the mite to
which the animal was not allergic (group A) or the mite
to which the animal was allergic (group B). Treatment
was shown to be more effective in group B. It can be
reasonably assumed that the same is true for other species of mite and hence, testing should involve different
species so that these different sources of allergens can
be included as necessary in the desensitization vaccine.
Secondly, demonstrating within a population of
atopic dogs, the presence of subgroups for which aeroallergens, especially mites, play a major role in the
development of skin lesions, also suggests that allergenic avoidance measures, instituted early on, might,
as has been shown in man,10,2628 lead to significant
improvement in canine atopic dermatitis.
Thirdly, some forage mite species have been found,
preferentially, in foods, especially dry commercial
diets.29 Avoiding this sort of food would be a logical
thing to propose when sensitivities to these species
have been demonstrated. However, a recent North
American study, using immunohistochemical techniques, found no evidence of Dermatophagoides spp.
(house dust mites) in high-quality commercial dry
diets.30 Further studies are necessary to confirm this
hypothesis.
2002 Blackwell Science Ltd, Veterinary Dermatology, 13, 39 44

CONCLUSION
This study increases our knowledge of environmental
allergen sensitivity patterns in the atopic dog. Results
confirm the necessity of a thorough allergy investigation, involving testing with allergenic extracts appropriate to the individual history of the patient, whenever
hyposensitization is needed. Further studies using
atopic patch tests are needed to allow the role of environmental allergens in the development of atopic dermatitis to be evaluated more fully.3134 Further studies
are also needed to determine the major allergens and
the epitopes responsible for sensitization to forage
mites, and to better appreciate the importance of crossreactions between different species of mites in the dog.

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controlled trial effect of house dust mite allergen avoidance on atopic dermatitis. Lancet, 1996; 347: 1518.
11. Deblay, F., Casel, S., Mbazoa-Amougou, C. Atopie et
environnement domestique. Revue Franaise Dallergologie 2000; 40: 11018.
12. Sture, G.H. Canine atopic disease. The prevalence of
intradermal skin testing at two sites in the North and
South of Great Britain. Veterinary Immunology and
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15. Hart, B.J. Ecologie et biologie des acariens allergniques.
In: Fain, A., Gurin, B., Hart, B.J., eds. Acariens etallergies. Varennes: Allerbio, 1988: 13042.
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17. Prlaud, P., Guagure, E., Alhaidari, Z. et al.
Rvaluation des critres de diagnostic de la dermatite
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18. Carlotti, D.N. Diagnostic allergologique in vivo, DAPP,
atopie, allergie alimentaire. In: Guagure, E., ed. Les
Indispensables de Dermatologie. Paris: PMCAC, 1991:
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19. Codner, E.C., Tinker, M.K. Reactivity to intradermal
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20. Noli, C., Bernardina, G., Willemse, T. The significance of
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Prevalence of specific IgE to storage mites (A. siro,
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Rsum Cette tude sest intresse aux rsultats des intradermoractions avec des extraits de six acariens des
poussires ou de stockage chez 150 chiens prsentant une dermatite atopique. 120 animaux (80%) ont prsent
au moins une raction positive. Les sensibilisations Dermatophagoides farinae sont les plus frquentes (108
chiens, soit 90% des chiens positifs et 72% des chiens atopiques). Les ractions positives aux autres acariens ne
sont pas rares (respectivement 32%, 35%, 30%, 27% et 23% des chiens positifs pour Dermatophagoides pteronyssinus, Acarus siro, Tyrophagus putrescentiae, Glyciphagus domesticus et Lepidoglyphus destructor). Les monosensibilisations D. farinae sont frquentes (57% des cas), mais les polysensibilisations sont trs frquentes pour
les autres acariens. Il existe cependant des cas de monosensibilisation D. pteronyssinus (5 cas), T. putrescentiae
(1 cas) et G. domesticus (1 cas). Des tudes supplmentaires sont ncessaires pour apprcier plus prcisment
le rle jou par ces diffrentes espces dacariens dans la dermatite atopique canine.
Resumen Este estudio investig las reacciones de la prueba intradrmica a los extractos de seis especies de caros
en 150 perros con dermatitis atpica. Al menos una reaccin positiva fue detectada en 120 animales (80%). Dermatophagoides farinae fue el que produjo un nmero superior de reacciones positivas (108 perros, 90% de los perros y el 72% de los perros atpicos mostrando reacciones positivas). Las reacciones positivas a otros caros no
fueron infrecuentes, con muchos perros positivos a Dermatophagoides pteronyssinus (32% de los perros testados),
Acarus siro (35%), Tyrophagus putrescentiae (30%), Glycyphagus domesticus (27%) y Lepidoglyphus destructor
(23%). La sensibilidad nicamente a D. farinae fue frecuente (57% de los casos), pero se vieron a menudo sensibilidades mltiples en los otros caros. Tambin se vieron casos de sensibilidad a un solo caro: D. pteronyssinus
(cinco casos), T. putrescentiae (un caso) y G. domesticus (un caso). Se necesitan ms estudios para apreciar con
mayor claridad el papel que juegan las diferentes especies de caro en la dermatitis atpica canina.
Zusammenfassung Diese Studie untersuchte die intradermalen Testreaktionen gegen Extrakte von 6 Milbenspezies bei 150 Hunden. Bei 120 Hunden (80%) wurde zumindest eine positive Reaktion gesehen. Dermatophagoides farinae zeigte die hchste Anzahl von positiven Reaktionen (108 Hunde, 90% der Hunde und 72% der
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E. Bensignor and D. N. Carlotti

atopischen Hunde zeigten positive Reaktionen). Positive Reaktionen gegen andere Milben waren nicht
ungewhnlich, viele Hunde testeten positiv auf Dermatophagoides pteronyssinus (32% der getesteten Hunde),
Acarus siro (35%), Tyrophagus putrescentiae (30%), Glycyphagus domesticus (27%) und Lepidoglyphus destructor
(23%). Sensitivitt ausschliesslich gegen D. farinae war hufig (57% der Flle), aber mehrere Sensitivitten
gleichzeitig wurden hufig bei anderen Milben gesehen: D. pteronyssinus (5 Flle), T. putrescentiae (ein Fall) und
G. domesticus (ein Fall). Weitere Studien sind ntig, um die genaue Rolle der verschiedenen Milbenspezies bei
der atopischen Dermatitis des Hundes einzuschtzen.

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