The prevalence of Trichophyton mentagrophytes and
Cheyletiella spp. in guinea pigs in Dutch petshops
Fig.1: Trichophyton mentagrophytes after 3 weeks on Sabouraud dextrose agar
Report
Kim van Avermaete – 3154475
Research project: September 2011 – March 2012
Supervisors: Dr. Ing. P. van Overgaauw & Dr. N.J. Schoemaker
Utrecht University
Abstract
Dermatophytes form a group of closely related fungi that can cause disease in animals and
man by invading hairs, skin and nails. They use keratin for their growth. Dermatophytosis is
an important zoonotic disease. The source of human infections usually originates from a
lower animal source and in some research projects Trichophyton mentagrophytes was the
most frequently isolated dermatophyte with the guinea pig as a main source.
Most guinea pigs infected with T. mentagrophytes are asymptomatic carriers and do not show
clinical signs. Skin lesions, which usually start on the head and then progress over the back,
flanks and limbs, however, do occur. These skin lesions are pruritic in guinea pigs, just as
they are in man, in which pruritus and the specific ‘ringworm’ lesion are the main symptoms.
Little is known about the number of infected guinea pigs (carriers and clinical cases) in the
Netherlands. Outside the Netherlands prevalence’s of 1.4% to 34.9% were found.
The aim of this study was to determine the prevalence of T. mentagrophytes in guinea pigs in
Dutch pet shops. 179 guinea pigs in 88 pet shops without skin lesions were examined.
In 17.3% of the guinea pigs and in 27.3% of the total number of pet shops T. mentagrophytes
was isolated. The A. benhamiae-complex was isolated in 29 of 31 positive guinea pigs and the
A. vanbreuseghemii-complex of the T. mentagrophytes-complex was isolated in 2 of the 31
positive guinea pigs.
T. mentagrophytes was predominantly found in the Northern and Western parts of the
Netherlands. Furthermore, neither a significant sex, breed or age predisposition, nor a
significant correlation of infection with T. mentagrophytes and hairtype, cage-occupation,
turnover-rate, origin, exchange of bowls and coupling/combining of animals were found.
Cheyletiella is an on the surface of the skin living mite, which is a common parasite in dogs,
cats and rabbits. Since it does not have extreme host specificity, it can also infect guinea pigs
and humans. Cheyletiella is an obligate parasite which completes its life cycle in
approximately 35 days on the skin surface. The mite is transmitted by direct contact. In
rabbits the severity of clinical signs ranges from asymptomatic to moderate. Since little is
known about the prevalence of the zoonotic ectoparasite Cheyletiella parasitovorax in Dutch
pet shops and this ectoparasite can enhance susceptibility for Trichophyton mentagrophytes
infections, the guinea pigs examined for Trichophyton mentagrophytes were also examined
for the presence of Cheyletiella, but no ectoparasites were found.
This study shows that in a quarter of the Dutch pet shops guinea pigs are being sold which are
a zoonotic risk of dermatophytosis in humans and that in Dutch petshops Cheyletiella is a
very uncommon parasite in guinea pigs.
Index
1. Introduction
1
2. Methods & Materials
- §2.1 Sampling
- §2.2 Culturing
- §2.3 Differentiation
- §2.4 Statistical evaluation
5
5
6
7
10
3. Results
-
§3.1 Trichophyton mentagrophytes
§3.2 Cheyletiella parasitovorax
12
12
16
4. Discussion
- §3.1 Trichophyton mentagrophytes
- §3.2 Cheyletiella parasitovorax
17
17
19
5. Conclusion
20
6. Advice
-
21
21
21
§6.1 General preventive measurements
§6.2 Measurements in case of a dermatophyte
7. Acknowledgements
23
8. References
24
9. Appendices
- Appendix 1
- Appendix 2
27
28
38
1. Introduction
Trichophyton mentagrophytes is a fungus which belongs to the dermatophytes. The
dermatophytes form a closely related group of pathogenic fungi, which occur worldwide and
can cause disease in animals and man.15,48,66
There are a lot of different dermatophytes, which can be classified into three anamorphic
(asexual) genera: Epidermophyton, Microsporum and Trichophyton, which together contain
over 40 species.3,15,25,44,66 New molecular analytical methods revealed that several
dermatophytes of the anamorph genera Trichophyton and Microsporum are also capable of
reproducing sexually. These forms are classified in the teleomorphic genus
Arthroderma.8,15,35,48,66 The confirmed teleomorphs of the zoophilic isolates of the T.
mentagrophytes complex are Arthroderma benhamiae, Arthroderma simii and Arthroderma
vanbreuseghemii.2,29,60,61 Most of the dermatophytes in guinea pigs and rabbits are associated
with A. benhamiae.20
Dermatophytes can invade the hair, nails and the stratum corneum of the skin of the living
host and use keratin for their growth.15,44,25 Infection occurs by direct contact with an infected
animal and indirect through fomites and infected epithelial debris in the environment.1,12,34,44
Under favorable conditions fomites can remain infectious for months or even years.12,34,59
The infectious form of dermatophytes are arthrospores which are released by fragmentation of
hyphae in keratinized structures and adhere to these superficial structures. This is followed by
germination and the production of hyphae. The latter then invade the stratum corneum or hair
follicles. Hydrolytic enzymes, such as keratinase, may aid in the invasion proces.15,25,34,44,64
Signs due to a dermatophyte infection may range from mild to severe as a consequence of the
host’s reaction to the metabolic products of the dermatophyte, the virulence of the infecting
species, the anatomic location of the infection and local environmental factors.48,64,66 The
animals most at risk are the young, aged, debilitated and immune suppressed animals.44 The
disease is often seen secondary to stressors40,48 and minor trauma. Inappropriate shampooing
and ectoparasites can also facilitate infection, while high environmental temperature and
humidity may contribute to a more severe infection.34,43,44
Animals and man poses various forms of defense mechanisms against an infection with a
dermatophyte. In animals grooming of the skin and coat may remove arthrospores.15,34 The
skin of humans and animals functions as a physical barrier, is exposed to UV light, and has a
low moisture condition which is unfavorable for fungal growth. In addition, the skin possesses
antifungal substances and a commensal microflora of saprophytic microorganisms competing
with the dermatophyte, thereby preventing colonization of the skin by dermatophytes.51,65
Furthermore there is continuous keratinization and epidermal proliferation with continuous
shedding of the stratum corneum with which the dermatophyte is be removed.65 It is assumed
that keratinocytes not only play a role in the physical barrier of the skin but also initiate a
cutaneous inflammatory reaction by releasing cytokines.4
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After passing the physical barriers the dermatophytes are encountered by phagocytes,
including macrophages, which are soon reinforced by the recruitment of large numbers of
neutrophils to the sites of infection.28 Macrophages and neutrophils mostly contribute to the
antifungal innate immune response through phagocytosis and direct pathogen killing.52 These
cells contain pattern recognition receptors (PRRs), including Toll-like receptors (TLRs) with
which they recognize pathogen associated molecular patterns (PAMPs).27,50,51 Recognition by
TLRs leads to the production of several important mediators of innate immunity, such as
cytokines and chemokines.37,39,54,62 The Toll pathway also leads to the surface expression of
co-stimulatory molecules that are essential for the induction of adaptive immune
responses.9,28,50
The cell mediated immune response is the main mechanism of defense against fungal
infections, but certain types of antibody responses may also play a role in the protection of the
host.42 Th1 cells predominantly produce cytokines such as IFN-y and promote cell mediated
immunity and phagocyte activation, thereby playing a role in the clearance of a fungal
infection. Th2 cells mainly produce cytokines such as interleukins 3 and 4 and tend to
promote antibody production. Th2 immunity usually results in susceptibility to infection or
allergic responses.7,9,13,62
According to their habitats and host preferences dermatophytes can be classified as geophilic,
zoophilic or antropophilic species. Geophilic species are saprophytes in soil and occasionally
cause disease in man; antropophilic and zoophilic species are obligatory parasites of which
the first normally infects animals but can also affect man and of which the latter only have
man as a host.1,64
Antropophilic fungi in man results in dermatophytosis which is mostly confined to protected
areas of the body. Dermatophytosis due to geophilic or zoophilic species, however, is
commonly found on exposed areas of the body (head, arms, legs). The antropophilic species
can cause insidious and chronic infections in humans, while the zoophilic species do not seem
to be able to cause such infections and usually result in much more acute inflammatory
infections.41,59,65 It has been suggested that there is a kind of inhibitor in the keratin of the
preferred host that ‘turns off ‘ the production of the inflammatory agents by the colonizing
fungus. When the fungus colonizes a different host, however, the inhibitor is lacking.48
Dermatophytosis is probably the most important zoonotic disease which is transmitted
directly from the animal to the person.5,41 The skin of humans who are infected can show the
development of one or more red circular lesions of limited size, which can coalesce. The
lesions can be localized on any part of the body. The head seems the most frequently
involved. In time, the lesions will become dry and scaly, whereby central healing is seen (the
classical form). In many infections, however, the entire area shows greater or less scaling.
Pruritus is a main symptom of dermatophytosis in man, while erythema, induration and
swelling are also seen.12,59
Infections caused by dermatophytes (ringworm) are classified according to their localization
on the body of the infected animal or human and by appending the Latin term designating the
body site after the word tinea, for example tinea capitis for ringworm of the scalp and tinea
corporis for ringworm of the body (trunk, shoulders or limbs).24,66
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Humans are usually infected by a lower animal source.41,55Alteras (1966) found that, in
patients suffering from dermatophytosis, the zoophilic dermatophyte Trichophyton
mentagrophytes is the dermatophyte most frequently isolated, with the guinea pig as its main
source.5 A few years earlier, the same results were described by Koch and Rieth
(1958).31Fumeaux (2004) found Arthroderma benhamiae of the T. mentagrophytes-complex
in 9 isolates of 8 children and 1 adult suffering from inflammatory dermatophytosis. Eight of
these individuals had had previous contact with rodents, mostly guinea pigs.18
In guinea pigs the dermatophyte most commonly isolated is Trichophyton
mentagrophytes.15,32,43,47,53,63 To a lesser extent Microsporum canis may also be found.5,47
Most of the guinea pigs infected with T. mentagrophytes show no clinical signs and are
asymptomatic carriers.15,63 Guinea pigs that do have symptoms, show skin lesions, which
usually start on the head and gradually progress over the back, the flanks and the limbs. These
lesions are often pruritic and can consist of focal circular areas of alopecia, scaling and
erythema.12,40,46
The best way to take samples of symptomatically infected animals is to take hairs from the
sides of the lesion. If crusts are present, a part of these should also be collected. Hairs must be
pulled out instead of cut off.26 Sampling of asymptomatic animals is best performed with the
Mackenzie’s toothbrush technique.53 With this technique, not only hairs but also keratin debris
is collected. This is especially useful as the hyphae may only be present in the stratum
corneum.26,57
The two media most frequently used to culture dermatophytes are the sabouraud dextrose agar
and the dermatophyte test medium (DTM).57
The sabouraud dextrose agar is the most widely used medium in medical mycology for the
isolation and routine subculture of most common fungal pathogens. It contains glucose,
peptones and agar.38
Bacteria and saprophytic fungi which colonize the skin and/or its hair/nails could interfere
with isolation of dermatophytes since dermatophytes grow more slowly. Therefore, media for
isolation of dermatophytes are supplemented with antibiotics (chloramphenicol, gentamycin)
and antimycotic cycloheximide, which prevents growing of saprophytic fungi.11
The DTM is a sabouraud dextrose agar, which contains cycloheximide, gentamicin and
chlortetracyclin as antifungal and antibacterial agents and phenol red as a pH indicator. The
medium contains protein and carbohydrates. The dermatophytes firstly use this protein as a
nutrient source of which the alkaline metabolites turn the medium from yellow to red.57,66
When the medium does not contain protein anymore, the dermatophyte starts to use
carbohydrates of which the acid metabolites turn the medium from red to yellow.57 White
mycelia growth and a color change to red within 10 days after inoculation is conclusive for
the presence of dermatophytes.15
There are some disadvantages of the dermatophyte test medium. The DTM must be evaluated
daily,15,57 which is impractical for this study as a lot of pet shops had to be visited. The red
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color change can also be due to nonpathogenic fungi and the DTM does not allow
visualization of colony reverse pigmentation, which is often important in identification.57,66
Since desiccation and ultraviolet light hinder growth,57 the plates should be packed in plastic
bags and incubated in the dark.
Little is known about the number of infected guinea pigs (symptomatically and
asymptomatically) in the Netherlands. The reported prevalence of T. mentagrophytes outside
of the Netherlands ranges from 1.4% to 34.9%.6,17,32,53,63
Since dermatophytosis is a common zoonotic disease which can easily be transferred from
guinea pigs to humans and the fact that T. mentagrophytes is one of the main etiologic agents
which is often found in guinea pigs, it was found important to know the prevalence of this
dermatophyte in guinea pigs in the Netherlands. Furthermore, guinea pigs are predominantly
sold to children who are more susceptible to an infection with dermatophytes than adults.22,59
In addition, the young animals which are sold are those most susceptible to infection with
dermatophytes.12,67 It would therefore be important to know what the prevalence of T.
mentagrophytes would be in young guinea pigs sold in pet shops.
The aim of this study was therefore to determine the prevalence of T. mentagrophytes in
guinea pigs in Dutch pet shops.
Cheyletiella
Cheyletiella is an on the surface of the skin living mite, which is a common parasite in dogs
(Cheyletiella yasguri),45 cats (Cheyletiella blakei),30 and in rabbits (Cheyletiella
parasitovorax).21,58,67 The various species do not have extreme host specificity and may also
infect guinea pigs and humans. In guinea pigs the mite is not seen very often.56,58,67
Cheyletiella is an obligate parasite which completes its life cycle in approximately 35 days on
the skin surface. The mite is transmitted by direct contact. They usually survive not longer
than 1-2 days away from the host.67
In rabbits the mite can cause crusts on the back, trunk and flanks. An increased scaling and
alopecia is often seen. The severity of clinical signs ranges from asymptomatic to
moderate.23,58 In man, Cheyletiella can give large numbers of intensely itchy papules with
necrotic areas on the places were there has been contact with the animal. There is even a case
report of cheyletiellosis with systemic manifestations.14
Since little is known about the prevalence of the zoonotic ectoparasite Cheyletiella
parasitovorax in Dutch pet shops and this ectoparasite can enhance susceptibility for
Trichophyton mentagrophytes infections,58 the guinea pigs examined for Trichophyton
mentagrophytes were also examined for the presence of Cheyletiella.
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2. Materials & Methods
2.1 Sampling
2.1.1 Pet shop selection
To determine the amount of pet shops which needed to be sampled throughout the
Netherlands a power-analysis was performed. The following assumptions were made: Total
amount of pet shops in the Netherlands (n= 1232). The expected prevalence of the diseases
was assumed at 5%; a confidence interval of 95% was used and an error of 5% was accepted.
Based on these assumptions a random sample of 69 pet shops was needed. To extend the
reliability of this research project, 125 pet shops were selected. A total of 91 shops were
cooperating, of which 3 did not sell Guinea pigs. Therefore, a total of 88 pet shops were
included in this study. None of the pet shops were notified in advance of the visit to prevent
extra measures taken by the shop, which could influence the outcome of the study. To get an
overview of T. mentagrophytes in part of the Netherlands, the provinces were also divided in
four groups of three provinces. The first consisted of Friesland, Groningen and Drenthe; the
second contained Overijssel, Gelderland and Flevoland; the third consisted of Utrecht and
Noord- and Zuid-Holland and the last group contained the provinces Zeeland, Noord-Brabant
and Zuid-Limburg.
2.1.2 Animals
In each pet shop a sample was taken from one guinea pig per cage that contained these
animals. The age, gender and hair type of every sampled animal was recorded. In addition, it
was recorded whether the animal was housed alone or with other guinea pigs and/or rabbits.
The type of bedding in the cage, as well as the first impression of the hygiene was also
recorded.
A total of 179 guinea pigs were examined (Table 2.1). Their age ranged from 4 weeks up to 2
years with a median age of 12 weeks (Table 2.4). Of all these animals 61.5% (110/179) was
male and 38.5% female (69/179) (Table 2.3). Of the guinea pigs 86.0% (154/179) was short
haired, 11.7% (21/179) had long hairs and 2.2% (4/179) did have hairs of medium length
(Table 2.5). Further more 36.9% (66/179) was housed solely, 34.6% (62/179) was housed
with 1 or more guinea pigs and 28.5% (51/179) with or without guinea pigs but with rabbits
(Table 2.6). In all of the pet shops and cages the first impression of the hygiene was good.
2.1.3 Questionnaire
Each owner of the pet shop was asked to fill out a questionnaire. Topics in the questionnaire
focused on the amount of guinea pigs sold on a yearly basis, the origin of the animals
(wholesale business/private sector/etc.), the presence of a veterinary policy, a protocol at time
of the arrival of the animals (preventive therapy) and their hygiene policy. The complete
questionnaire can be found in Appendix 1.
In the results the following factors and their influence on infection with T. mentagrophytes are
being worked out separately: age, gender, hair-type, cage-occupation, turn-over rate, supplier,
exchange of animals and exchange of bowls.
-5-
A possible correlation between percentages of infection and the different provinces will also
be worked out.
2.1.4 Sample taking
The Mackenzie’s toothbrush technique was used in all animals whereby the entire body of the
guinea pig was brushed during one minute with a new toothbrush.26,57
The toothbrushes were then placed in a paper bag and closed with a staple. All bags were
preserved in a large plastic bag.
To determine if the animals were infected with Cheyletiella parasitovorax, the animals were
brushed with a flee comb36 and the hairs and scales from this comb were examined in light
with a magnifying glass (the mites are 270 – 540 µm36). When there was doubt about whether
the ectoparasite was present or not, the comb was tapped on a white paper and examined with
the magnifying glass again.
2.2 Culturing
2.2.1 Media
For this study sabouraud B dextrose agar plates were used. These plates contained peptic
digest of animal tissue 5.0g/l; pancreatic digest of casein 5.0g/l; dextrose 40.0g/l; agar 15.0g/l;
Inositol 10.0g/l; Cycloheximide 0.2g/l; Vitamin B 1.0g/l and Depomycin 3.0g/L.
2.2.2. Culture
Contents of each toothbrush was cultured within 1-7 days (Table 2.11) after sampling. The
brushes were gently pressed onto the sabouraud dextrose agar. When the brush also contained
hair and scales, these were taken by sterile tweezers and inoculated on the agar plate.
The plates were incubated in the dark for 3 weeks at 25 °C.
The plates were checked for growth of T. mentagrophytes on a weekly basis. When no fungal
growth was seen within three weeks, the culture was considered negative.
Plates containing colonies, which were suspected to be T. mentagrophytes, were examined at
one week post inoculation to count the amount of colonies present. At a later stage colonies
could coalesce, making it impossible to count them anymore.
Suspected colonies were subcultured in the dark on a malt extract agar (MEA) plate for three
weeks at 25 °C in a plastic bag. The MEA plate was used to cultivate, isolate and enumerate
T. mentagrophytes. After one to three weeks when the MEA plate contained pure growth, a
preparation of a small part of a colony was made and stained with blue lactic acid to visualize
the macro- and microconidia of T. mentagrophytes. These preparations were examined under
the microscope with a magnification of 853.3.
After one or two weeks when the MEA plate showed a mixed culture instead of a pure
culture, a new MEA plate was inoculated with part of the colony from the sabouraud plate or
the MEA plate and incubated again for three weeks.
-6-
2.3. Differentiation
In this research project the differentiation of T. mentagrophytes happened by means of colonic
growth morphology, specific microscopic findings and PCR.
2.3.1. Morphology24
The colonies of T. mentagrophytes on a Sabouraud dextrose agar plate are often star-shaped.
They are powdery to floccose. The colonies have a cream to yellowish color. The down side
often has an ochre to red-brown color, occasionally a yellow or dark brown color is observed.
(For M. canis the colonies have a spreading and radiating shape. They are woolly. The
colonies have a grayish- to tannish-white color. The down side is deep ochraceous-yellow).
Fig.2: Trichophyton mentagrophytes after 1 week on Sabouraud dextrose agar
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Fig.3: Trichophyton mentagrophytes after 3 weeks on Sabouraud dextrose agar
Fig. 4: Trichophyton mentagrophytes after 3 weeks on Sabouraud dextrose agar (down side)
-8-
2.3.2. Microscopy24
With microscopy of a preparation of T. mentagrophytes from a MEA plate, microconidia and
macroconidia could be observed. The macroconidia are usually sparse. They are 3-8 celled
and 20-50 x 6-8µm in size. They have smooth and thin walls, and are clavate to cigar-shaped.
The microconidia are frequently present. They have a spherical shape and are arranged in
dense, grape-like clusters or arranged alongside the hyphae.
The hyphae are frequently present. They are spiral formed, and are 2 µm in diameter.
(For M. canis the macroconidia are 6-12 celled and 35-110 x 12-25 µm in size. They have
rough and thick walls with thinner septa. They are spindle-shaped, with a slightly bent,
verrucose, rostrate apex. The microconidia have a clavate to pyriform form, and are arranged
alongside undiffertiated hyphae.)
Fig. 5: Microscopic preparation of T. mentagrophytes (sigar-shaped macroconidia)
Fig.6: Microscopic preparation of T. mentagrophytes (grape-like structures with microconidia)
2.3.3 Molecular analyses
The best way to confirm that the colony on a plate is actually T. mentagrophytes is the use of
molecular analyses.20 Martin Meijer BSc of the CBS isolated the DNA of the agents growing
on the plates of which was thought under the microscope that they may contain T.
mentagrophytes. Because there was a maximum on the number of cultures of which we could
-9-
analyze DNA, we chose to do a PCR of one culture of every positive shop. There were two
shops in which we had two different cultures, of these shops a PCR of both cultures was done.
2.3.3.1 DNA isolation
1. 300µl Microbead solution was added to a Microbead tube
2. 50µl MD1 was also added
3. The colony was scraped from the culture with an inoculation loop
4. The Microbead tubes were shortly put in the vortex
5. The Microbead tubes were vortexed with the MO Bio adapter for 10 minutes
6. The tubes were centrifuged at room temperature for 1 minute, RPM=9600
7. 100µl MD2 was added to 2ml tubes and the supernatant was added to these tubes
8. These tubes were vortexed for 5 seconds
9. These 2ml tubes were put on ice for a few minutes
10. The 2ml tubes were centrifuged for 1 minute, RPM=9600
11. The supernatant was added to new sterile 2ml tubes and to these tubes 900µl MD3 was
added
12. The 2ml tubes were gently mixed with a pipette
13. 700µl of the 2ml tubes with supernatant was added on the spin filters, which than were
centrifuged for 1 minute, RPM=9600
14. The filters were than gentle pulled out of the tubes, the supernatant was removed, after
which the filters were put back into the tubes
15. The residual supernatant of step 13 was added on the spin filters
16. These were centrifuged for 1 minute, RPM=9600
17. The filters were gently pulled out of the tubes, the supernatant removed and the filters
put back to the tubes
18. 300µl MD4 was added to the spin filters and this was centrifuged for 1 minute,
RPM=9600
19. The filters were then again pulled out of the tubes, the supernatant removed and the
filters put back in the tubes, which were centrifuged for 1 minute, RPM=9600
20. The spin filters were pulled out of the tubes and added to new 2ml tubes
21. 50µl MD5 was added in the middle of the spin filter in the new 2ml tubes
22. These new tubes were centrifuged for 1 minute, RPM=9600
23. The tubes were left for a few minutes at room temperature
24. The spin filters were thrown away and the tubes with DNA stored at -20°C
2.3.3.2 PCR
Of every tube a PCR was done by Martin Meijer BSc of the Centraal bureau voor
schimmelcultures. A specific set of primers of dermatophytes was added.
2.4 Statistical evaluation
All the collected data were added in excel and SPSS. The computer program SPSS was used
to do the statistics of this research project. An independent samples T-test was used to
determine if the mean age of guinea pigs on which T. mentagrophytes was found significantly
deviates from the mean age of guinea pigs free from T. mentagrophytes.
- 10 -
The Chi-Square test was used to test if there was a correlation between infection with T.
mentagrophytes and the province where the animals came from, the age-groups, the gender
and hair type of the animals, the cage-occupation, the turnover of the shop, the origin of the
animals and whether exchange of bowls and coupling/combining of animals of different cages
took place. When a significant correlation was found, a Cramer’s V value was determined.
- 11 -
3. Results
3.1. Trichophyton mentagrophytes
No clinical cases of dermatophytosis were seen in any of the pet shops visited.
3.1.1. Questionnaire
Based on the questionnaire 12.8% (23/179) came from shops where there were less than 20
guinea pigs sold per year, 34.6% (62/179) came from shops where they sell 21-50 guinea pigs
per year, 33.0% (59/179) came from shops where they sell 51-100 guinea pigs per year and
19.6% (35/179) of the animals lived in shops where they yearly sell more than 100 guinea
pigs (Table 2.7).
A total of 28.5% (51/179) of the animals lived in shops where the animals were always
supplied by wholesaler’s, 6.7% (12/179) was examined in shops where wholesaler’s only
sometimes were used as suppliers and the greatest part of the animals, 64.8% (116/179) was
examined in shops that never used wholesaler’s as their suppliers (Table 2.8). A percentage of
73.2% (131/179) of the animals was housed in shops where there was no exchange of bowls
between the cages and 26.8% (48/179) of the animals lived in shops where there was
exchange of bowls (Table 2.10). At last 75.4% (135/179) of the animals was housed in shops
where the staff sometimes coupled or combined animals (Table 2.9).
3.1.2. Samples
3.1.2.1. Morphology (Table 3.4)
Of the 179 samples taken, 41 showed growth that could resemble T. mentagrophytes on the
sabouraud agar and were transferred to the malt extract agar plates after 1-2 weeks. 32 of
them were still suspected of being T. mentagrophytes on the base of morphology after two to
three weeks of growth on sabouraud dextrose agar plates. These 32 cultures came from a total
of 24 shops.
3.1.2.2. Microscopy
After two or three weeks of growth on the malt extract agar plates, a preparation of these 32
malt extract agar plates with suspected cultures was made and were examined under the
microscope. After de microscopy only one culture could be considered negative.
3.1.2.3 PCR
After morphologic and microscopic examination only 31 cultures were left. A PCR confirmed
that they contained T. mentagrophytes.
In 22 of the 24 pet shops (91.7%) in which T. mentagrophytes was found the Arthroderma
benhamiae complex of T. mentagrophytes was isolated and in 2 of these pet shops (8.3%) the
Arthroderma vanbreuseghemii complex of T. mentagrophytes was isolated.
Based on the similarity of the morphologic and microscopic appearance and the fact that some
infected animals lived in the same shop, this corresponds to 29 (93.5%) with Arthroderma
benhamiae infected guinea pigs and 2 with Arthroderma vanbreuseghemii infected guinea
pigs (6.5%).
- 12 -
3.1.3. Statistics
3.1.3.1 Prevalence’s
T. mentagrophytes was found on 31 of the 179 examined guinea pigs, which corresponds to
17.3% of the animals (Table 3.5).
T. mentagrophytes was isolated on Guinea pigs in 24 of the 88 pet shops examined, resulting
in a prevalence of T. mentagrophytes in Dutch pet shops of 27.3%.
3.1.3.2 Statistics
Provinces (Table 3.1-3.3, 3.6-3.12)
Province
Visited
Positive
shops
shops
Groningen
Friesland
Drenthe
Overijssel
Gelderland
Noord-Brabant
Zuid-Limburg
Zeeland
Zuid-Holland
Noord-Holland
Utrecht
Flevoland
5
6
3
14
13
9
3
3
18
9
4
1
Percentage +
in province
on total
shops visited
in province
(%)
80.0
16.7
0.0
21.4
7.7
11.1
33.3
100.0
16.7
55.6
50.0
0.0
4
1
0
3
1
1
1
3
3
5
2
0
Percentage
+ on total
shops
visited (%)
Percentage
+ on total
+ shops
(%)
4.6
1.1
0.0
3.4
1.1
1.1
1.1
3.4
3.4
5.7
2.3
0.0
16.7
4.2
0.0
12.5
4.2
4.2
4.2
12.5
12.5
20.8
8.3
0.0
Table 3.1: Percentages of positive shops per province (%)
The percentages of positive shops per province differed from 0% to 100%, the percentages of
positive shops per province on the total amount of shops visited, range from 0% to 5.7% and
the percentages of positive shops per province on the total number of positive shops differ
from 0% to 20.8% (Table 3.1).
- 13 -
Province
Groningen
Friesland
Drenthe
Overijssel
Gelderland
Noord-Brabant
Zuid-Limburg
Zeeland
Zuid-Holland
Noord-Holland
Utrecht
Flevoland
Chi-Square: 35.13, significance 0.00
Percentage of positive guinea pigs (%)
22.6
9.7
0.0
16.1
3.2
3.2
3.2
9.7
9.7
16.1
6.5
0.0
Cramer V 0.44
Table 3.2: Percentage of positive guinea pigs per province
There is a significant correlation, although it is not a strong one (Cramer V 0.44), between the
percentage of positive guinea pigs and the provinces (Table 3.2). Most of the positive guinea
pigs were found in Groningen followed by Noord-Holland and Overijssel.
Province-group
Percentage of positive guinea pigs (%)
Friesland, Groningen, Drenthe
Overijssel, Gelderland, Flevoland
Utrecht, Noord- en Zuid-Holland
Zeeland, Noord-Brabant, Zuid-Limburg
Chi-Square: 10.55, significance 0.01
32.2
19.4
32.3
16.1
Cramer V 0.24
Table 3.3: Percentage of positive guinea pigs per province-group
T. mentagrophytes was more often found in the Northern and Western parts of the
Netherlands than it was found in the South and Eastern parts of the Netherlands (Table 3.3).
As the Cramer V value was 0.24, this is not a strong significant correlation.
Gender (Table 3.13-3.14)
T. mentagrophytes was found on 15.5% of all male and on 20.3% of all female guinea pigs.
54.8% of the positive guinea pigs were male and 45.2% were female guinea pigs.
There is not a significant correlation between the gender of the guinea pigs and infection with
T. mentagrophytes.
Age (Table 3.33-3.38)
The mean age of the guinea pigs on which T. mentagrophytes was found was 14.1 weeks and
the mean age of the negative guinea pigs 18.8 weeks. The significance level of the
independent samples T-test was 0.18, so there is not a significant deviation between the mean
age of the positive and the negative group of guinea pigs.
- 14 -
When the guinea pigs which had an age of 78 weeks or more were left out, the mean age of
the guinea pigs on which T. mentagrophytes was found was 12 weeks and the mean age of the
negative guinea pigs 14.8 weeks. The significance level of this independent samples T-test
was 0.12, so also in this case there is not a significant deviation between the mean age of the
positive and the negative group of guinea pigs.
When the guinea pigs which had an age of 52 weeks or more were left out, the outcomes were
a mean age of 12 weeks for positive guinea pigs, 13.9 weeks for negative guinea pigs with a
significance level of 0.19 so no significant deviation between the mean age of the positive and
the negative group of guinea pigs.
Hair type (Table 3.15 & 3.16)
T. mentagrophytes was found on 17.5% of the short haired guinea pigs, on 14.3% of the
guinea pigs with long hairs and on 25% of the guinea pigs with medium hairs.
90.3% of the positive guinea pigs was short haired, 6.5% had long hairs and 3.2% had hairs of
a medium length. There was no significant correlation between infection with T.
mentagrophytes and hair type of the guinea pigs.
Cage-occupation (Table 3.17 & 3.18)
T. mentagrophytes was found in 19.7% of the guinea pigs that were housed solely, in 17.7%
of the animals which were housed with other guinea pigs and in 13.7% of the guinea pigs
which were housed with rabbits and with or without other guinea pigs.
41.9% of the positive guinea pigs were housed solely, 35.5% were housed with other guinea
pigs and 22.6% were housed with rabbits and with or without other guinea pigs. There was no
significant correlation between the cage-occupation and infection with T. mentagrophytes.
Turnover (Table 3.19 & 3.20)
T. mentagrophytes was found in 17.4% of the guinea pigs from shops with a turnover of less
than 20 guinea pigs per year, in 16.1% of the guinea pigs from shops with a turnover of 21-50
guinea pigs per year, in 13.6% of the guinea pigs from shops with a turnover of 51-100 guinea
pigs per year and in 25.7% of the guinea pigs from shops with a turnover of more than 100
guinea pigs per year.
87.1% of the positive guinea pigs came from shops with a turnover of more than 20 guinea
pigs per year.
There was no significant correlation between the turnover of the shops and infection with T.
mentagrophytes.
Origin (Table 3.21-3.22; 3.27-3.32)
T. mentagrophytes was found in 19.6% of the guinea pigs that were supplied by wholesaler’s,
in 17.2% of the guinea pigs that came from shops that never used wholesaler’s as suppliers
and in 8.3% of the guinea pigs that came from shops that sometimes used wholesaler’s as
suppliers.
64.5% of the positive guinea pigs came from shops that never used wholesalers as suppliers of
their animals.
- 15 -
There was no significant correlation between occurrence of dermatomycosis and
supplementation by wholesalers.
To find out if there is a relation between the provinces with the highest percentage of
infection (Groningen, Noord-Holland and Overijssel) and supplying by wholesalers in these
provinces the Chi-Square test was used.
28.5% of all the guinea pigs came from shops that used wholesalers as their suppliers. It is
remarkable that 94.1% (16/17) of the guinea pigs which were sampled in Noord-Holland
came from shops that only used wholesalers as their supplier. 31.4% of the total number of
shops which used wholesalers were located in Noord-Holland. A significant correlation
between the provinces and the use of wholesalers as suppliers (Chi-Square of 136.36,
significance level of 0.00, Cramer’s V of 0.62) was found.
To find out if there is a relation between the province-groups with the highest percentage of
infection (Northern and Western parts of the Netherlands) and supplying by wholesalers in
these parts the Chi-Square test was used.
One of the 27 guinea pigs (3.7%) sampled in the northern part of the Netherlands, 14 of the 65
guinea pigs (21.5%) sampled in the eastern part of the Netherlands, 27 of the 53 guinea pigs
(50.9%) sampled in the western part of the Netherlands and 9 of the 34 guinea pigs sampled
in the southern part of the Netherlands came of shops which used only wholesalers as their
suppliers. 52.9% of the total guinea pigs which were supplied by wholesalers were sampled in
the western part of the Netherlands (Noord- &Zuid- Holland and Utrecht).
A significant correlation between the province-groups and the use of wholesalers as suppliers
(Chi-square of 39.0, significance level of 0.00, Cramer’s V of 0.33) was found.
Bowl-exchange (Table 3.23 & 3.24)
T. mentagrophytes was found in 18.3% of the guinea pigs that came from shops where no
bowl exchange took place and in 14.6% of the guinea pigs that came from shops were bowl
exchange did take place.
77.4% of the positive guinea pigs came from shops where no exchange of bowls between the
cages took place.
There was no significant correlation between infection with T. mentagrophytes and bowlexchange.
Coupling/Combining of guinea pigs (Table 3.25 & 3.26)
T. mentagrophytes was found in 18.1% of the guinea pigs that came from shops where
coupling or combining of animals took place and in 17.0% of the guinea pigs that came from
shops where coupling or combining of animals did not take place.
74.2% of the positive guinea pigs came from shops that did not couple or combine animals.
There was no significant correlation between coupling/combining of animals and infection
with T. mentagrophytes.
3.2. Cheyletiella
As shown in Table 2.1, the fur mite was detected on none of the examined guinea pigs.
- 16 -
4. Discussion
4.1. Trichophyton mentagrophytes
In this first study into the prevalence of T. mentagrophytes in Dutch pet shops, this fungus
was detected on Guinea pigs in 27.3% of the visited pet shops. The prevalence in pet shops
turned out to be higher than the estimated prevalence of 5% that was presumed for the power
analysis performed prior to the study.17,58,63 All the positive guinea pigs were asymptomatic
carriers. Because this dermatophyte has zoonotic potential it is good to know that T.
mentagrophytes can be present without noticing it and that this might be the case more often
than assumed. Shop owners should be aware of this fact so that they may send their customers
to their doctor if symptoms of ringworm appear after buying a new pet.
T. mentagrophytes was found in 17.3% of the guinea pigs. This is a higher percentage than
was found in previous studies where the prevalence of T. mentagrophytes in asymptomatic
guinea pigs ranged from 1.4 to 13% (amount of animals per study ranged from 63 to 222).6,
17,53,63
The fact that in this study T. mentagrophytes was found is not surprising because in guinea
pigs this is the dermatophyte most commonly isolated.15,32,43,47,53,63
It is to be expected that laboratory animals have a lower prevalence of T. mentagrophytes
compared to pet animals. The latter may explain why in some of the previous studies, which
included laboratory guinea pigs, an overall lower prevalence was found. The higher
prevalence found in this research project could also be due to a prevalence difference of
dermatophytes between countries.67
Kraemer, however, retrospectively used 1132 specimens collected from guinea pigs in 395
(34.9%) of which T. mentagrophytes was found. These specimens were collected from three
different laboratories. Except from all states in Germany, a small number of samples also
originated from Austria, Italy, Luxembourg, the Netherlands and Switzerland. One laboratory
received specimens of animals suspected of dermatophytoses. In this laboratory 251 of 584
(43%) of the specimens were positive for T. mentagrophytes. In the other two laboratories T.
mentagrophytes was found in 27% (105/383) and 23.6% (39/165) of the cases.32
In the second part of this study healthy pet guinea pigs, guinea pigs with skin diseases and
guinea pigs with diseases not affecting the skin were evaluated prospectively. This resulted in
a prevalence of 8.5%, 7.7% and 8.0%, respectively.
In 91.7% of the positive pet shops and in 93.5% of the guinea pigs on which T.
mentagrophytes was found, the Arthroderma benhamiae complex of T. mentagrophytes was
isolated. The Arthroderma vanbreuseghemii complex of T. mentagrophytes was isolated in
8.3% of the positive pet shops and in 6.5% of the positive guinea pigs. This is consistent with
the findings of Gräser, who reported that both complexes can be found on guinea pigs and
strains of the A. benhamiae complex are very likely to have rabbits and guinea pigs as a more
restricted range of host species.20 No relationship was found between the two shops in which
- 17 -
A. vanbreuseghemii was cultured, as they were located many kilometers (235 km) apart and
they did not share the same suppliers.
In this study no gender predisposition was found, which is consistent with previous reports on
T. mentagrophytes in guinea pigs and other wild rodents.19,32,33
Younger animals seem more susceptible to an infection, which can be due to a stronger
immunity in older animals because they had more contacts with fungi12 or because they have
an insufficiently developed immune system and smaller amounts of fungistatic fatty acids in
their sebum.40,63,67
The mean age of the guinea pigs on which T. mentagrophytes was found was 14 weeks and
the mean age of the guinea pigs with a negative culture was 19 weeks. Of the animals which
were over 26 weeks of age 5.6% and of the animals which were younger than 26 weeks of age
18.6% were positive for T. mentagrophytes.
A total of 96.8% of the positive guinea pigs in this study was younger than 26 weeks. This
outcome is influenced by the fact that mainly younger animals were sampled, but similar
findings were encountered by other researchers. They found that all the infected guinea pigs
were less than six months of age63 and the affected animals were significantly younger than
the animals with negative cultures.32 Furthermore, in one research project a higher mortality
rate in young guinea pigs infected with Trichophyton mentagrophytes during an epizootic
outbreak of T. mentagrophytes was found.43
We did not find a significant correlation between infection and hair type. Thus, in this study a
breed predisposition for T. mentagrophytes is not found. This is consistent with other reports
which commonly also do not mention a breed predisposition, except for the report of Van
Geel, in which is stated that all of the four guinea pigs which were found positive for T.
mentagrophytes were short haired.63
In this study no significant correlation was found between the cage occupation, the turnover
of the shop, the origin of the animals, the bowl-exchange between the cages and
coupling/combining of animals on the one side and infection with T. mentagrophytes on the
other side (Table 3.28 – 3.37).
Guinea pigs are social animals, which live in groups. Individual housing may therefore result
in stress, which in turn could possibly influence the immune response and make individually
housed guinea pigs more susceptible to an infection. This also counts for housing with too
many animals in a small cage.
In this study there was not a great difference in percentages of positive animals between
solely housed animals and guinea pigs that were housed with congeners. This could be due to
the fact that in most shops the animals in the same cage had the same origin and
combining/coupling with animals of different origin was seldom done. This reduces the risk
of cross infection. Further more overcrowding was barely seen. Some guinea pigs fight with
each other or are left on their own when the other animals in their cage are sold, in these
- 18 -
cases, combining or coupling of the guinea pigs, if health and welfare are concerned, are good
decisions.
Infection between cages via fomites could of course also occur.1,12,34,44 This, however, is not
very likely, because in 95.5% of the shops just one cage with guinea pigs was positive for
Trichophyton mentagrophytes and most of the positive guinea pigs came from shops were the
food and water bowls were not exchanged. In these shops cleaning and feeding of the cages
was done one cage at a time, whereby all attributes of one cage were placed back into the
same cage before starting with the next.
The lowest infection was seen in guinea pigs that were also housed with rabbits. The fact that
rabbits seem no greater source of infection is consistent with our own study (unpublished
data) and other studies, in which was found that guinea pigs are more often carriers of T.
mentagrophytes32 and that rabbits are more resistant to infections with dermatophytes.6,17,53
A shop which sells more guinea pigs per year has more supply and thus introduction of new
young guinea pigs, which could be a source of infection, in the shop. Even so, if more animals
need to be cleaned and handled, it could be the case that they get less attention and care and
the risk of cross infection may be higher due to a bit more time-dependent carelessness.
This research did not show a significant correlation between the turnover of the shop and
infection with T. mentagrophytes, but the highest percentage of positive guinea pigs were
found in shops with a turnover of more than 100 (25.8% against 17.4; 16.1 and 13.6%).
It should be noticed that most of the owners gave an estimation of their turnover rates and that
the turnover is seasonally influenced. Most of the animals are sold in the summer. The shops
mostly have less guinea pigs and less supply of guinea pigs during winter, in which season
this research project took place. For this reason it could be interesting to repeat this study
during summer.
The assumption that T. mentagrophytes would be isolated more on guinea pigs that were
supplied by wholesalers, is not confirmed by this study. Over 60% of the positive guinea pigs
came from shops that never used wholesalers as animal suppliers.
4.2. Cheyletiella
No fur mite was detected on any of the guinea pigs that were examined. This is probably due
to the fact that the mite does not infect guinea pigs very often56,58 and most of the animals
were getting preventive therapy with ivermectine, which is also effective in combating
Cheyletiella-infections before they were put into the cage.36,58
- 19 -
5. Conclusion
Trichophyton mentagrophytes was found in 17.3% of the examined guinea pigs in Dutch pet
shops. The present study showed that guinea pigs in Dutch pet shops could be carriers of T.
mentagrophytes without showing lesions or clinical signs and that the dermatophyte is present
in 27.3% of the Dutch pet shops. Because this dermatophyte has zoonotic potential and
because it has guinea pigs, which are often bought as children’s pets, as its main carriers,
further research is needed to reveal factors influencing the prevalence of T. mentagrophytes in
pet shops so that in future preventive measurements can be taken to decrease this percentage.
- 20 -
6. Advise
We wrote an advice about how to deal with dermatophytes in a pet shop and we sent every
cooperating pet shop a copy.
6.1. General preventive measurements
Cleaning and disinfection of the cages must be done before arrival of new animals and by
appearance of the disease. All the bedding must be removed and all surfaces and cageattributes must be cleaned. After these two steps disinfection can take place, with a solution of
bleach/chloride in water23 or with a solution of halamid (sodium p-tolueensulfonchlooramid)
in water. After the disinfection the cages should be rinsed well with water to prevent burning
skin lesions in the animals.
Newly arrived animals should be checked for (skin)lesions and should be washed with
imaverol. It is wise to keep newly arrived animals apart for a while because they could bear
diseases with them. In case of (skin)lesions all newly arrived animals should be kept apart of
the animals that are already present.
Since guinea pigs are frequent carriers of dermatophytes, they should be kept apart from
rabbits to prevent infecting the latter animals.
Stress should be avoided. Prevention of overcrowding and individual housing and giving them
the comfort of good food and a possibility to hide prevents stress.47
General measures to prevent spreading of the disease in the shop are important. The cages
should be kept apart, water and food bowels should stay with the same animals. Before
switching of to another cage, the hands of the staff should be disinfected. Infected and ill
animals should be touched and fed after the healthy animals are done. Customers should not
be allowed to touch the animals.
6.2. Measurements in case of a dermatophyte infection
In case of a dermatophyte-infection, the supplier should always be informed. Although the
infected animal has already been sold, it is still possible that the dermatophyte is still present
in the shop. Therefore all the cages should be cleaned and disinfected as mentioned at the
general preventive measurements, followed by treatment of the cages with enilconazole
(Imaverol concentrate). This should be diluted in water (10ml emulsion/L water). The cages
should be left to dry on air or can be dried with a hairdryer. While treating the cage, gloves
should be worn.
The animals that are still present in the shop should be washed with imaverol. The animals
that show skin lesions or the animals of which is confirmed that they are carriers of the
dermatophyte should be kept apart. These animals should be sent back to the supplier.
The infected animals that are already sold should be treated with itraconazol (rabbit 5-10
mg/kg,23 guinea pig 5mg/kg) every 24 hour for 4-6 weeks.10,49
From these animals a culture should be made every month to determine if they are still
infected. The treatment should be continued until two successive cultures are negative. In
practice treatment during 1 month seems enough to eliminate the dermatophyte.
- 21 -
We also informed the owners of the pet shops about the zoonotic character of the
dermatophytes and that immune-compromised humans are more at risk. Hands and clothes
should be washed thoroughly after touching the animals.
- 22 -
7. Acknowledgements
Many thanks to Dr. Nico Schoemaker, Utrecht University and Dr. Ing. Paul van Overgaauw,
Institute for Risk Assessment Sciences for their support during this research project and to
Angele Timan and Ali Eggenkamp for all their help and support with obtaining the Sabouraud
B agar plates and usage of the incubator.
I also would like to thank Martin Meijer BSc. and Prof. Dr. Dr. h. c. R A Samson of the CBSKNAW Fungal Biodiversity Centre for their time, support, leads and help in the
differentiation and isolation of Trichophyton mentagrophytes.
The Dibevo (Amersfoort, Netherlands) are acknowledged for sponsoring this research project
and for providing the addresses of all pet selling shops in the Netherlands.
Finally I would like to thank all the cooperating pet shops for the warm welcome, their time
and interest and their cooperation.
- 23 -
8. References
1. Ajello, L., 1962. Present day concepts in the dermatophytes. MycopatholMycolAppl 17:315-324
2. Ajello, L., Cheng, S.L., 1967. The perfect state of Trichophyton mentagrophytes. Sabouraudia
5:230-234
3. Ajello, L., 1968. A taxonomic review of the dermatophytes and related species. Medical
Mycology, 6(2):147-159
4. Almeida, S.R., 2008. Immunology of Dermatophytosis. Mycopathologia 166:277-283
5. Alteras, I., 1966. Human dermatophyte infections from laboratory animals. Medical Mycology
4:143-145
6. Balsari, A., Bianchi, C., Cocilovo, A., Dragoni, I., Poli, G., Ponti, W., 1981. Dermatophytes in
clinically healthy laboratory animals. Laboratory Animals 15:75-77
7. Bellochio, S., Bozza, S., Montagnoli, C., Perruccio, K., Gaziano, R., Pitzurra, L., Romani, L.,
2005. Immunity to Aspergillus fumigates: the basis for immunotherapy and vaccination. Med
Mycol 43: (Suppl.I), S181-S188
8. Berbee, M.L., Taylor, J.W.: Fungal phylogeny, in Oliver R.P., Schweizer, M. (eds): Molecular
Fungal Biology. Cambridge University Press, 1999, pp 21-77
9. Blanco, J.L., Garcia, M.E., 2008. Immune response to fungal infections. Veterinary Immunology
and Immunopathology 125:47-70
10. Borgers, M., Xhonneux, B., Van Cutsem, J., 1993. Oral itraconazole versus topical bifonazole
treatment in experimental dermatophytosis. Mycoses 36:105-115
11. Bulajic, N.M., Ivanovic, D.M., Savic, M.Z., 2005. Modified sabouraud dextrose agar for isolation
and identification of dermatophytes. Proc Nat Sci, MaticaSrpska Novi Sad 108:291-299
12. Chermette, R., Ferreiro, L., Guillot, J., 2008. Dermatophytoses in animals. Mycopathologia
166:385-405
13. Crameri, R., Blaser, K., 2002. Allergy and immunity to fungal infections and colonization.
EurRespir J 19:151-157
14. Dobrosavljevic, D.D., Popovic, N.D., Radovanovic, S.S., 2007. Systemic manifestations of
Cheyletiella infestation in man. International Journal of Dermatology 46:397-399
15. Donnelly, T.M., Rusha, E.M., Lacknera, P.A., 2000. Ringworm in small exotic pets. Semin Avian
Exot Pet 9:82-93
16. Drouot, S., Mignon, B., Fratti, M., Roosje, P., Monod, M., 2009. Pets as the main source of two
zoonotic species of the Trichophyton mentagrophytes complex in Switzerland, Arthroderma
vanbreuseghemii and Arthroderma benhamiae. Vet Dermatol 10: 13-18
17. Feuerman, E., Alteras, I., Hönig, E., Lehrer, N., 1975. Saprophytic occurence of Trichophyton
mentagrophytes and Microsporum gypseum in the coats of healthy laboratory animals.
Mycopathologia 55:13-15
18. Fumeaux, J., Mock, M., Ninet, B., Jan, I., Bontems, O., Lechenne, B., Lew, D., Panizzon, R.G.,
Jousson, Ol, Monod, M., 2004. First report of Arthrodermabenhamiae in Switzerland.
Dermatology 208:244-250
19. Gallo, M.G., Lanfranchi, P., Poglayen, G., Calderola, S., Menzano, A., Ferroglio, E., Peano, A.,
2005a. Seasonal 4-year investigation into the role of the alpine marmot (Marmotamarmota) as a
carrier of zoophilic dermatophytes. Med Mycol 43:373-379
20. Gräser, Y., Scott, J., Summerbell, R., 2008. The new species concept in dermatophytes – a
polyphasic approach. Mycopathologia 166:239-256
21. Griffiths, H.J., 1971. Some common parasites of small laboratory animals. Laboratory Animals
5:123-135
22. Hay, R.J., 1992. Fungal skin infections. Arch Dis Child 67(9):1065-1067
- 24 -
23. Hess, L.: Dermatologic diseases, in Quesenberry, K.E., Carpenter, J.W. (eds): Ferrets, Rabbits,
and Rodents. Elsevier, 2004, pp 194-202
24. Hoog de, G.S., Guarro, J., Gené, J., Figueras, M.J. Atlas of clinical fungi, 2nd edition. 2000. Pp
10, 22-23, 743-745, 968-970
25. Hosking, S.: Fungi as animal pathogens, in Oliver R.P., Schweizer, M. (eds): Molecular Fungal
Biology. Cambridge University Press, 1999, pp 322-340
26. Houwers, D.J., Blankenstein, B., 2009. Het diagnostisch mycologisch onderzoek.
Diergeneeskundig memorandum 2:58-66
27. Janeway Jr., C.A., Medzhitov, R., 2002. Innate immune recognition. Ann Rev Immunol 20:197216
28. Janeway Jr., C.A., Travers, P., Walport, M., Shlomchik, M.J.: Immunobiology, the immune
system in health and disease. Garland science, 2005, pp 37-80
29. Kano, R., Yamada, T., Makimura, K., Kawasaki, M., Mochizuki, T., Kamata, H., Hasegawa, A.,
2011. Arthroderma benhamiae(The Teleomorph of Trichophyton mentagrophytes) Mating TypeSpecific Genes. Mycophathologia 171:333-337
30. Keh, B., Lane, R.S., Shachter, S.P., 1987. Cheyletiellablakei, an ectoparasite of cats, as cause of
cryptic arthropod infestations affecting humans. West J Med 146:192-194
31. Koch, H., Rieth, H., 1958. Endemische Trichophytie bei Meerschweinchen. Archivfür klinische u.
experimentelle Dermatologie 205:577-585
32. Kraemer, A., Mueller, R.S., Werckenthin, C., Straubinger, R.K., Hein, J., 2011. Dermatophytes in
pet Guinea pigs and rabbits. Veterinary Microbiology, doi:10,1016/j.vetmic.2011.12.005
33. Lewis, E., Hoff, G.L., Bigler, W.J., Jefferies, M.B., 1975. Public health and the urban gray
squirrel: mycology. J Wildl Dis11:502-504
34. Lloyd, D.H., Immunopathogenesis of dermatophytosis. 16th Annual Congress of the European
Society of Veterinary Dermatology (ESVD) and the European College of Veterinary Dermatology
(ESVD), Helsinki, Finland, August 12-14, 1999
35. Mahmoud, A., Ghannoum, Nancy, C., Isham: Dermatophytes and dermatophytoses, in Elias, J.,
Anaissie, M.D., Michael, R., McGinnis, PhD, Michael, A. Pfaller, M.D. (eds): Clinical Mycology.
Churchill Livingstone, 2009, pp 375-384
36. Mellgren, M., Bergvall, K., 2008. Treatment of rabbit cheyletiellosis with selamectin or
ivermectin: a retrospective study. ActaVeterinariaScandinavica 50:1, doi:10.1186/1751-0147-50-1
37. Murphy, P.M., Baggiolini, M., Charo, I.F., Hebert, C.A., Horuk, R., Matsushima, K., Miller, L.H.,
Oppenheim, J.J., Power, C.A., 2000. International Union of Pharmacology. XXII. Nomenclature
for chemokine receptors. Pharmacol Rev 52:145-176
38. Odds, F.C., 1991. Sabouraud(‘s) agar. Journal of Medical and Veterinary Mycology 29:355-359
39. O’garra, A., McEvoy, L.M., Zlotnik, A., 1998. T-cell subsets: chemokine receptors guide the way.
CurrBiol 8:646-649
40. O’Rourke, D.P.: Disease Problems of Guinea Pigs, in Quesenberry, K.E., Carpenter, J.W. (eds):
Ferrets, Rabbits, and Rodents. Elsevier, 2004, pp 245-254
41. Pier, A.C., Smith, J.M.B., Alexiou, H., Ellis, D.H., Lund, A., Pritchard, R.C., 1994. Animal
ringworm – its aetiology, public health significance and control. Journal of Medical and
Veterinary Mycology 32:133-150
42. Polonelli, L., Casadevall, A., Han, Y., Bernadis, F., Kirkland, T.N., Matthews, R.C., Adriani, D.,
Boccanera, M., Burnie, J.P., Cassone, A., Conti, S., Cutler, J.E., Frazzi, R., Gregory, C., Hodgetts,
S., Illidge, C., Magliani, W., Rigg, G., Santoni, G., 2000. The efficacy of acquired humoral and
cellular immunity in the prevention and therapy of experimental fungal infections. Med Mycol 38
(Suppl.1): 281-292
- 25 -
43. Pombier, E.C., Kim, J.C., 1975. An epizootic outbreak of ringworm in a guinea-pig colony caused
by Trichophytonmentagrophytes. Lab Anim 9:215-221
44. Quinn, P.J., Markey, B.K., Carter, M.E., Donnelly, W.J., Leonard, F.C.: Dermatophytes, in
Veterinary Microbiology and Microbial Disease. Blackwell science, 2002, pp 224-228
45. Rack, G., 1971. Cheyletiellayasguri Smiley, 1965 (Acarina, Cheyletiellidae),
einfakultativmenschenpathogenerParasit des Hundes. Z Parasitenk 36:321-334
46. Richardson, V.C.G., Diseases of Domestic Guinea pigs. Blackwell Science, 2000, pp 1-2
47. Rigby, C., 1976. Natural infections of guinea-pigs. Laboratory animals 10:119-142
48. Rippon, J.W.: Cutaneous infections, in Wonsiewicz, M. (ed.): Medical Mycology: The Pathogenic
Fungi and the Pathogenic Actinomycetes. W.B. Saunders Company, 1988, pp 169-185, 224-236
49. Rochette, F., Engelen, M., VandenBossche, H., 2003. Anitfungal agents of use in animal health –
practical applications. J. vet. Pharmacol. Therap. 26:31-53
50. Roeder, A., Kirschning, C.J., Rupec, R.A., Schaller, M., Weindl, G., Korting, H.C., 2004. Tolllike receptors as key mediators in innate antifungal immunity. Med Mycol 42:485-498
51. Romani, L., 2004. Immunity to fungal infections. Nat Rev Immunol 4:1-13
52. Romani, L., 2011. Immunity to fungal infections. Nat Rev immunol 11:275-288
53. Rosenthal, S.A., Wapnick, H., 1963. The value of mackenzie’s “hair brush” technic in the
isolation of T. mentagrophytes from clinically normal guinea-pigs. J Invest Dermatol 41:5-6
54. Rossi, D., Zlotnik, A., 2000. The biology of chemokines and their receptors. Annu Rev Immunol
18:217-242
55. Sarkisov, A. Kh., Koromyslov, G. Proposals for the prevention and control of dermatophytoses
common to man and animals. WHO/ISHAM Consultation on Dermatophytoses Common to Man
and Animals. Palmerston North, New Zealand, 6-7 February 1982. WHO Document VPH/82.35
56. Scarff, D.H., 1991. Skin disorders of small mammals. Journal of Small Animal Practice 32:408412
57. Scott, D.W., Miller, W.H., Griffin, C.E.: Diagnostic methods, in Muller & Kirk (eds.): Small
Animal Dermatology. Saunders, 2000, pp 118-125
58. Scott, D.W., Miller, W.H., Griffin, C.E.: Parasitic Skin Disease, in Muller & Kirk (eds.): Small
Animal Dermatology. Saunders, 2000, pp 429, 453-457
59. Smith, J.M.B.: Superficial and Cutaneous Mycoses, in Hubbert W.T., McCulloch, W.F.,
Schnurrenberger, P.R. (eds): Diseases Transmitted from Animals to Man. Charles C Thomas
Publisher, 1975, pp 469-487
60. Stockdale, P.M., Mackenzie, D.W.R., Austwick, P.K.C., 1965. Arthroderma simii sp. nov., the
perfect state of Trichophyton simii (Pinoy) comb. nov.Sabouraudia 4:112-123
61. Takashio, M.: The Trichophytonmentagrophytes Complex, in Iwata K. (ed): Recent advances in
medical and veterinary mycology. University Park Press, 1977, pp 271-275
62. Traynor, T.R., Huffnagle, G.B., 2001. Role of chemokines in fungal infections. Med Mycol 39:4150
63. Vangeel, I., Pasmans, F., Vanrobaeys, M., De Herdt, P., Haesebrouck, F., 2000. Veterinary Record
146:440-441
64. Vermout, S., Tabart, J., Baldo, A., Mathy, A., Losson, B., Mignon, B., 2008. Pathogenesis of
Dermatophytosis. Mycopathologia 166:267-275
65. Wagner, D.K., Sohnle, P.G. 1995. Cutanous Defenses against Dermatophytes and Yeasts.
ClinMicrobiol Rev 8:317-335
66. Weitzman I., Summerbell R.C., 1995. The dermatophytes. ClinMicrobiol Rev 8:240-259
67. Yager, J.A., Scott, D.W.: The skin and appendages, in Jubb, K.V.F., Kennedy, P.C., Palmer, N.
(eds): Pathology of Domestic Animals. San Diego, Academic Press, 1993, pp 661-664, 686
- 26 -
9. Appendices
Appendix 1 (Chapter 2)
- Table 2.1: Examined guinea pigs
- Frequency tables 2.2 - 2.10
- Questionnaire
- Table 2.11 : Dates of sampling and culturing
28
32
35
36
Appendix 2 (Chapter 3)
- Table 3.4 : Amount of suspected colonies after 1 week
- Table 3.5: Percentage of guinea pigs with T. mentagrophytes
- Table 3.6: Percentages of positive shops per province (%)
- Cross-Tables & Chi-Square Tests 3.7 – 3.32
- Independent samples T-test 3.33 – 3.38
38
39
39
40
49
- 27 -
Appendix 1
Table 2.1 Examined guinea pigs
Specimen
1C
2B
3B
3C
3E
4E
5B
5C
5D
5E
7F
7G
7H
8C
9A
10B
11B
12B
12C
12E
13B
13C
16A
16C
17B
17D
18C
19A
19D
19E
20A
20B
21A2
22A
23A
24B
24D
25C
25E
25F
26B
26C
Gender
♂
♀
♂
♂
♀
♀
♂
♂
♂
♀
♀
♀
♀
♀
♂
♀
♂
♀
♂
♂
♀
♀
♀
♂
♀
♀
♂
♀
♂
♂
♀
♂
♂
♀
♀
♀
♂
♂
♂
♀
♂
♂
Hair length
Long
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Medium
Short
Short
Short
Long
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Long
Short
Short
Short
Short
Age (wks)
Cage
occupation*
10
6
4
9
5
7
20
38
10
52
24
16
12
16
10
10
16
8
10
36
78
78
6
6
12
14
14
10
10
10
16
16
104
6
7
7
9
12
7
4
10
10
S
MS
SS
SS
SS
SS
S
S
SS
S
S
S
S
S
MS
SS
S
SS
MS
MS
S
S
MS
MS
SS
SS
S
S
SS
S
S
S
MS
SS
MS
SS
S
MS
MS
SS
MS
S
- 28 -
Cheyletiella
-
Hygiene
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
27E
27F
28D
29B
30C
30D
31B
31C
32A
33A
33B
33C
34A
35B
36A
36B
36D
36E
37A
37E
37F
38B
38C
39A
39B
39C
40C
40D
41D
41E
42AX
42B
43A
43B
43C
44B
44C
44D
44F
44G
45A
45B
46D
46E
46F
47B
47E
47F
48A
48C
♀
♂
♂
♀
♂
♀
♂
♀
♂
♀
♂
♂
♂
♀
♀
♀
♀
♂
♂
♀
♂
♀
♂
♂
♂
♂
♂
♂
♂
♂
♂
♂
♂
♂
♀
♂
♀
♀
♂
♂
♂
♂
♂
♀
♂
♂
♀
♂
♂
♂
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Long
Short
Short
Long
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Long
Short
Short
Short
Short
Long
Long
Long
Short
Long
Short
Short
Medium
Long
Long
Short
Short
Short
Short
Short
Short
Short
Long
5
8
9
10
13
18
6
12
10
11
7
12
14
16
78
10
78
78
12
10
8
9
10
18
16
16
8
52
11
8
5
52
16
16
16
26
14
5
14
8
8
12
6
6
10
9
9
26
26
26
SS
SS
SS
SS
S
S
SS
SS
S
MS
MS
MS
SS
S
SS
MS
S
SS
SS
SS
S
SS
S
S
S
S
MS
SS
MS
MS
MS
S
S
S
S
MS
MS
MS
MS
SS
SS
MS
SS
SS
SS
SS
S
S
MS
MS
- 29 -
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
48D
49E
49F
50B
50D
50E
51C
52A
53A
53C
54A
55B
56A
56C
56D
57B
58B
59A
59C
60A
60C
60E
61A
61B
61D
61G
62D
63A
63B
63C
63G
64A
65D
66A
66D
67B
68A
68B
69B
69E
69F
70A
70B
71C
72A
73E
73F
74A
74B
75A
♂
♂
♂
♂
♀
♂
♂
♂
♂
♂
♀
♀
♀
♂
♀
♂
♂
♀
♂
♀
♂
♂
♂
♂
♀
♂
♂
♀
♂
♂
♂
♂
♂
♂
♀
♂
♂
♀
♂
♀
♂
♂
♂
♂
♂
♂
♀
♂
♀
♀
Long
Medium
Short
Short
Short
Short
Short
Short
Short
Long
Short
Short
Short
Short
Short
Long
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Medium
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Long
Long
Short
Short
Short
Short
26
18
18
9
11
12
26
26
12
10
15
5
26
12
12
10
10
8
8
13
26
11
36
26
26
26
15
8
7
16
12
36
9
26
26
10
9
6
10
10
10
9
9
5
36
26
26
14
8
11
MS
S
S
SS
S
SS
SS
S
SS
SS
S
SS
SS
S
MS
MS
MS
MS
MS
S
MS
SS
S
SS
SS
S
SS
MS
SS
S
S
S
MS
SS
SS
SS
SS
SS
S
SS
S
SS
MS
S
SS
S
MS
SS
S
SS
- 30 -
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
11
20
20
20
11
11
8
8
10
12
14
14
8
8
12
12
78
78
78
8
8
78
26
10
10
16
26
26
26
20
16
5
15
10
16
20
6
*S=Solely, SS=Same Species, MS=Mixed Species
75E
76A
76B
76D
77A
77B
78B
79A
80A
80E
80F
80G
80H
81B
82D
82E
83A
83C
83F
83G
84A
85B
85D
86A
86C
87B
87C
87E
88A
88C
88D
89B
89C
90C
90D
90E
91A
♂
♂
♀
♂
♀
♂
♀
♀
♂
♀
♂
♂
♀
♂
♀
♂
♂
♂
♂
♀
♂
♂
♀
♀
♀
♀
♀
♂
♀
♂
♀
♂
♂
♂
♂
♀
♀
S
MS
S
MS
S
SS
MS
MS
S
SS
S
S
SS
SS
SS
SS
S
S
S
SS
S
MS
SS
MS
S
MS
MS
MS
MS
MS
MS
MS
MS
S
S
S
S
Short
Short
Short
Short
Long
Short
Short
Short
Short
Short
Long
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Short
Long
Short
Short
Short
Short
Short
- 31 -
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Frequency tables
Table 2.2: Total number of guinea pigs
Table 2.3: Male and female percentages of the random sample (%)
Table 2.4: Age in weeks of the examined guinea pigs
Table 2.5: Hair type of the examined guinea pigs
- 32 -
Table 2.6: Cage-occupation of the examined guinea pigs
Table 2.7: Amount of guinea pigs sold per year
Table 2.8: Origin of the guinea pigs
Table 2.9: Coupling/Combining of the guinea pigs
Table 2.10: Bowl-exchange between cages
- 33 -
- 34 -
Questionnaire

How many guinea pigs are sold in this pet shop per year?
 50
 100
 150
 200
 250
 300
 Different, …

What is the origin of the bought animals?
 Wholesale
 Private
 Different, …

What’s the veterinary policy in the pet shop?
 Is there a vet who visually checks the animals on a certain moment?Yes/No
 Are the animals get a preventive therapy before they entering their cages?
Yes/No
 How?
 With?

How is the hygiene policy in the shop?
 How many times are the cages cleaned? With?
 Are the eat- and drink bowls of different cages exchanged or do they always stay
in the same cage?
Firm/Exchange
 Are animals being moved to other cages or mixed when they didn’t arrive
together?
Yes/No

What is the size of the cages in m2?

What is the knowledge of the employees?
 Which diplomas?

Are the employees familiar with the term ‘Zoonosis’?
Familiar/Not familiar

Is the shop recognized by StichtingDierbaar?
Yes/No
- 35 -
Table 2.11 Dates of sampling and culturing
Shop
1
2
3
4
5
6*
7
8
9
10
11
12
13
14*
15*
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
Sampling
03-11-2011
03-11-2011
09-11-2011
10-11-2011
10-11-2011
15-11-2011
15-11-2011
15-11-2011
16-11-2011
16-11-2011
17-11-2011
22-11-2011
22-11-2011
22-11-2011
23-11-2011
23-11-2011
23-11-2011
29-11-2011
29-11-2011
30-11-2011
30-11-2011
30-11-2011
01-12-2011
01-12-2011
01-12-2011
06-12-2011
06-12-2011
06-12-2011
06-12-2011
07-12-2011
07-12-2011
07-12-2011
08-12-2011
08-12-2011
08-12-2011
08-12-2011
09-12-2011
13-12-2011
14-12-2011
14-12-2011
14-12-2011
15-12-2011
15-12-2011
15-12-2011
Culturing
09-11-2011
09-11-2011
10-11-2011
10-11-2011
10-11-2011
18-11-2011
18-11-2011
18-11-2011
18-11-2011
18-11-2011
18-11-2011
25-11-2011
25-11-2011
25-11-2011
25-11-2011
25-11-2011
25-11-2011
02-12-2011
02-12-2011
02-12-2011
02-12-2011
02-12-2011
02-12-2011
02-12-2011
02-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
09-12-2011
16-12-2011
16-12-2011
16-12-2011
16-12-2011
16-12-2011
16-12-2011
16-12-2011
- 36 -
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
91
15-12-2011
20-12-2011
20-12-2011
21-12-2011
21-12-2011
21-12-2011
21-12-2011
22-12-2011
22-12-2011
04-01-2012
05-01-2012
05-01-2012
10-01-2012
10-01-2012
10-01-2012
12-01-2012
12-01-2012
12-01-2012
12-01-2012
17-01-2012
17-01-2012
17-01-2012
17-01-2012
17-01-2012
18-01-2012
18-01-2012
18-01-2012
18-01-2012
18-01-2012
24-01-2012
24-01-2012
24-01-2012
24-01-2012
24-01-2012
24-01-2012
24-01-2012
25-01-2012
25-01-2012
25-01-2012
25-01-2012
25-01-2012
26-01-2012
26-01-2012
26-01-2012
02-02-2012
02-02-2012
02-02-2012
16-12-2011
23-12-2011
23-12-2011
23-12-2011
23-12-2011
23-12-2011
23-12-2011
23-12-2011
23-12-2011
06-01-2012
06-01-2012
06-01-2012
13-01-2012
13-01-2012
13-01-2012
13-01-2012
13-01-2012
13-01-2012
13-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
20-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
27-01-2012
03-02-2012
03-02-2012
03-02-2012
*These shops didn’t have guinea pigs, just rabbits
- 37 -
Appendix 2
Table 3.4: Amount of suspected colonies after 1 week
Specimen
Amount of suspected colonies after 1 week
2B
Countless
8C
20
11B
20
32A
20-30
36D
30-40
53A
Countless
54A
5
55B
40
63A
15
63B
40-50
63C
7
68A
Countless
68B
5
69B
Countless
69E
43
69F
6
70A
1
70B
4
71C
Countless
73E
3
76A
1
77A
2
77B
6
81B
16
83G
14
84A
3
85D
Countless
86A
4
87B
3
88A
1
90C
8
90D*
2
*This sample turned out not to be T. mentagrophytes after microscopic examination
- 38 -
Percentages of shops & guinea pigs with T. mentagrophytes
Table 3.5: Percentage of guinea pigs with T. mentagrophytes
Table 3.6 Percentages of positive shops per province (%)
Province
Visited
shops
Positive
shops
Percentage +
(%) in
province
Percentage
+ on total
(%)
Groningen
Friesland
Drenthe
Overijssel
Gelderland
Noord-Brabant
Zuid-Limburg
Zeeland
Zuid-Holland
Noord-Holland
Utrecht
Flevoland
5
6
3
14
13
9
3
3
18
9
4
1
4
1
0
3
1
1
1
3
3
5
2
0
80,0
16,7
0,0
21,4
7,7
11,1
33,3
100,0
16,7
55,6
50,0
0,0
4,55
1,14
0,00
3,41
1,14
1,14
1,14
3,41
3,41
5,68
2,27
0,00
- 39 -
Percentage
+ on total
+ shops
(%)
16,67
4,17
0,00
12,50
4,17
4,17
4,17
12,50
12,50
20,83
8,33
0,00
Cross-Tables & Chi-Square tests
Table 3.7 & 3.8: Cross-Table & Chi-Square of the Provinces
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Table 3.9: Cramer’s V value of the Chi-Square of the Provinces and Infection
Table 3.10 & 3.11: Cross-Table & Chi-Square of Province-groups
Table 3.12: Cramer’s V value of the Chi-Square of the Province-groups & Infection
- 41 -
Table 3.13 & 3.14: Cross-Table & Chi-Square of Gender
- 42 -
Table 3.15 & 3.16: Cross-Table & Chi-Square of Hair-type
Table 3.17 & 3.18: Cross-Table & Chi-Square of Cage-occupation
- 43 -
Table 3.19 & 3.20: Cross-Table & Chi-Square of Turnover
Table 3.21 & 3.22: Cross-Table & Chi-Square of Origin
- 44 -
Table 3.23 & 3.24: Cross-Table & Chi-Square of Bowl-exchange
- 45 -
Table 3.25 & 3.26: Cross-Table & Chi-Square of Coupling/Combining of guinea pigs
- 46 -
Table 3.27 & 3.28: Cross-Table & Chi-Square of Provinces and Origin
- 47 -
Table 3.29: Cramer’s V value of the Chi-Square of provinces & origin
Table 3.30 & 3.31: Cross-Table & Chi-Square of Province-groups and Origin
Table 3.32: Cramer’s V value of the Chi-Square of the province-groups & origin
- 48 -
Independent samples T-test
Table 3.33: Group statistics
Table 3.34: Independent samples test
Table 3.35: Group statistics (without guinea pigs older than 1.5 year)
Group Statistics
Infected
N
Mean
Std. Deviation
Std. Error Mean
+
30
11,97
5,980
1,092
-
139
14,75
9,332
,792
age in weeks
Table 3.36: Independent samples test (without guinea pigs older than 1.5
year)
- 49 -
Table 3.37: Group statistics (without guinea pigs older than 1 year)
Group Statistics
Infected
N
Mean
Std. Deviation
Std. Error Mean
+
30
11,97
5,980
1,092
-
136
13,93
7,583
,650
age in weeks
Table 3.38: Independent samples test (without guinea pigs older than 1 year)
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