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CLINICAL CASE

Strongyloides stercoralis hyperinfection in

an immunosuppressed dog from
France,,
M. Cervone a,, A. Giannelli b, D. Otranto b, S. Perrucci a

a
Medicine University of Pisa, Department of Veterinary, Viale delle Piagge 2, 56124 Pisa, Italy
b
Medicine University of Bari, Department of Veterinary, Str. prov. per Casamassima km 3,
70010 Valenzano (Bari), Italy

Received 2 March 2016; accepted 6 May 2016

KEYWORDS Summary Strongyloides stercoralis is a threadworm, whose adult females parasitize the small
Strongyloides intestine of mammals causing severe clinical presentations in immunosuppressed animals and
stercoralis; puppies. A 10-month-old male Chihuahua dog was referred due to chronic diarrhoeic haema-
Hyperinfection tochezia, hematemesis, weight loss, pruritus and cough. During the clinical examination, severe
syndrome; weight loss and alopecia on the abdomen were observed. Stool examinations revealed the
Immunosuppressed presence of alive larvae of S. stercoralis, as well as cysts and trophozoites of Giardia duo-
dog; denalis. The negativity to S. stercoralis infection was achieved only after administration of
Concomitant ivermectin. Results of this study conrm that routine copromicroscopic methods may fail to
giardiosis diagnose S. stercoralis infection. In addition, although fenbendazole is considered the drug of
choice for the treatment of canine strongyloidiasis, ivermectin may be a valid alternative.
2016 AFVAC. Published by Elsevier Masson SAS. All rights reserved.

Crdits de formation continue. La lecture de cet article ouvre droit 0,05 CFC. La dclaration de lecture, individuelle et volontaire,

est effectuer auprs du CNVFCC (cf. sommaire).

The work was done at Small Animal Veterinary Clinic Paris III, Paris, France.
Authors declare off-label use of ivermectin (use of drug in a non approved category of animal). A blood test to detect the genetic

mutation responsible for the ivermectin sensitivity in dog (MDR1) was performed.
Corresponding author. Small Animal Veterinary Clinic Paris III, 17, boulevard des Filles-du-Calvaire, 75003 Paris, France.

E-mail addresses: mariocervone@live.it (M. Cervone), giannelli.alessio@gmail.com (A. Giannelli), domenico.otranto@uniba.it

(D. Otranto), stefania.perrucci@unipi.it (S. Perrucci).

http://dx.doi.org/10.1016/j.anicom.2016.05.001
2214-5672/ 2016 AFVAC. Published by Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Cervone M, et al. Strongyloides stercoralis hyperinfection in an immunosuppressed
dog from France. Revue vtrinaire clinique (2016), http://dx.doi.org/10.1016/j.anicom.2016.05.001
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VETCLI-41; No. of Pages 5 ARTICLE IN PRESS
2 M. Cervone et al.
Introduction
Intestinal parasites of dogs comprise a number of species
of zoonotic concern (e.g., Toxocara canis, Ancylostoma
spp.), including Strongyloides stercoralis Bavay, 1876 [1,2].
Parthenogenetic females of this nematode live threaded
in the epithelium of the small intestine in dogs, cats
and primates [3]. They produce eggs which hatch inside
the intestine in rst stage larvae (L1s). Hosts shed L1s
(and sometimes eggs) in their faeces. In the environment,
S. stercoralis L1s may then develop either to the infective
third-stage larvae (L3s) or moult into free-living adult nema-
todes, mainly depending on environmental conditions [1].
In the latter case, after mating, females produce eggs that
hatch into L1s [1,3], mature into infective L3s and are able
to infect a new susceptible host in which migrate to the
small intestine via lungs and, after two additional moults,
they develop to parthenogenetic adult females. The infec-
tion by S. stercoralis occurs percutaneously and, rarely, per
os. Infection through lactation (mainly between the rst and
third day post-birth) has been described but remains con-
troversial [4]. In addition, in immunosuppressed animals,
autoinfections may occur spontaneously with potential dis-
semination of migrating L3s through the intestinal wall or the
perianal skin [1,5]. In the infected host, strongyloidosis may
result in self-curing, acute and chronic forms supported by
autoinfection, and hyperinfection [6,7]. Difference between
chronic form and hyperinfection depends on the severity of
clinical manifestations and the number of adults in the intes-
tine. Indeed, hosts chronically infected are asymptomatic
or exhibit only minor symptoms; while hyperinfection is
more likely related with severe gastrointestinal and respi-
ratory alterations [7,8]. Severe forms are usually associated
with immunosuppressive or debilitating disorders in human
patients [7], but they are observed in young dogs with no
know factors of immunodeciency.
The prevalence of canine strongyloidiasis is underre-
ported, probably because of the diagnostic limitation due to
the uctuations in amount of larvae excreted in the faeces
[6,9]. Indeed, the parasitological diagnosis of S. stercoralis
infection is based on the Baermann test, the agar plate
method of Koga [10] or on the direct smear of fresh faeces
[11]. In asymptomatic patients, a single stool examination
fails to detect larvae in up to 70% of cases, so repeated
stool examination are required to increase diagnostic sensi-
tivity. Baermann method and especially agar plate method
of Koga are more sensitive than direct smear to detect larvae
in faeces [7]. However, due to lack of standard procedures in
most parasitology laboratories and low sensitivity of direct
parasitological methods, serological tests are also employed
[6,12], including indirect uorescent antibody (IFA) test
[13], an intradermal reaction test and radial immunodiffu-
sion [13,14].
S. stercoralis is commonly diagnosed in dogs from tropi-
cal and subtropical areas [15] with prevalence up to 24.3%
in Asia [16]. In Europe, canine strongyloidosis has been
reported in Germany [17], Finland [1], Greece [18], Portu-
gal [19] and Italy [20,21] with an overall mean prevalence
of about 0.8% [20].
The aim of the present paper is to describe a case
of S. stercoralis hyperinfection in an immunosuppressed
dog from France, coinfected by Giardia duodenalis. Data
Please cite this article in press as: Cervone M, et al. Strongyloides stercoralis hyperinfection in an immunosuppressed
dog from France. Revue vtrinaire clinique (2016), http://dx.doi.org/10.1016/j.anicom.2016.05.001
recorded would clarify the spectrum of the clinical con-
sequences and importance of diagnostic methods for this
zoonotic infection.
Observation
A 10-month-old male Chihuahua dog of 1.5 kg bodyweight
(Body Condition Score 2/9, according to WSAVA, Global
Nutrition Committee), purchased in an animal-shop in Paris
(France), was referred to a veterinary clinic because of
chronic diarrhoeic haematochezia, hematemesis, weight
loss and pruritus over a period of six months. Dur-
ing the previous week, the owner also reported that
the dog suffered for persistent respiratory abnormali-
ties and cough. Faecal examinations by otation test,
X-rays and abdominal ultrasounds were performed two
months before and any abnormality was recorded. There-
fore, inammatory bowel disease (IBD) was suspected
and the animal was put under regime of an intestinal
diet (I/D, Hills), an antidiarrhoeic-antibacterian association
(Canidiarix ; TVM, Lempdes, France; i.e., sulfaguani-
dine 50 mg/kg/day + framycetine 8.4 mg/kg/day + atropine
0.0021 mg/kg/day for 5 days, repeated three times with
an unknown interval), prednisone (Dermipred ; SOGEVAL,
Laval, France) 1 mg/kg/day for two months and a nutri-
tional complement (FortiFlora ; Purina, Missouri, USA),
but no improvement in clinical condition was observed.
Additionally, two months before the dog was referred,
a treatment with fenbendazole 50 mg/kg/day (Panacur ;
Intervet, Angers, France) for three days was performed and
repeated 15 days later, based on suspected intestinal proto-
zoan infection.
During the clinical examination, severe weight loss and
alopecia on the abdomen were the only physical alter-
ations observed. Blood tests revealed hypoalbuminaemia
(2.3 g/dL), increased level of alanine aminotrasferase
(ALT, 345 IU/L), anaemia (Hct, 28.82%), basal cortisol lev-
els < 5.52 nmol/L and low eosinophil percentage of 1.20%.
Radiographic examination of the thorax revealed the pres-
ence of exudative uid in the peri-ilar region, associated
to bronchogram. The image of striking bronchial pattern
associated with an alveolar pattern was compatible with
diagnosis of severe exudative or haemorrhagic pulmonary
disease. Abdominal ultrasound was then performed with a
57.5 MHz convex probe (EASEOTE-MyLabTM 25Gold, Maas-
tricht, Netherlands) in order to examine the intestinal tract,
but no signicant abnormalities were found. A fresh faecal
sample was collected and promptly analysed by otation
test with a low-density solution (specic gravity 1.2), by
direct smear and by the Baermann method. Stool examina-
tions revealed alive L1s of S. stercoralis (Fig. 1A and B) and
cysts and trophozoites of G. duodenalis. A real-time PCR of
the material collected via oro-pharyngeal brushing revealed
the presence of Bordetella bronchiseptica. Therefore, the
diagnosis of intestinal co-infection by S. stercoralis and
Giardia intestinalis was posed, associated with pulmonary
infection by B. bronchiseptica and iatrogenic Cushing syn-
drome. The dog was hospitalised and patient received IV
NaCl 0.9% uids (108 mL/day) and SC maropitan citrate
(Cerenia , PFIZER, Sandwich kent, UK, 1 mg/kg/day), in
order to restore normal hydration and to stop emesis
 Strongyloides stercoralis hyperinfection in an immunosuppressed dog from France

VETCLI-41; No. of Pages 5

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dog from France. Revue vtrinaire clinique (2016), http://dx.doi.org/10.1016/j.anicom.2016.05.001
Please cite this article in press as: Cervone M, et al. Strongyloides stercoralis hyperinfection in an immunosuppressed

Table 1 Clinical alterations, treatment and occurrence of parasites of the infected dog during the clinical follow-up.
Day 12 Day 34 Day 56 Day 7 Day 8 Day 910 Day 1113 Day 1416
Clinical signs Abdominal Mucous Cough, Cough, Cough, Pruritus Pruritus Loose

ARTICLE IN PRESS
pain, hem- diarrhoea, pruritus pruritus pruritus stools
orrhagic cough,
diarrhoea, pruritus,
vomiting, vomiting
anorexia,
cough,
pruritus
Treatment Citrate Sucralfate, Sucralfate, Fenbendazole, Metronidazole Metronidazole, Ivermectin Ivermectin
maropi- fenbenda- fenbenda- metronida- ivermectin
tant, zole, zole, zole,
metronida- metronida- metronida- amoxi-
zole, zole, zole, cilline
amoxi- amoxi- amoxi-
cilline, cilline, cilline
NaCl 0.9% NaCl 0.9%
Presence of parasites S.s. and S.s. and S.s. and S.s. S.s.
G.d. G.d. G.d.
Dosages, routes and period of administration are reported in the text. S.s.: Strongyloides stercoralis; G.d.: Giardia duodenalis; : negative.

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Figure 1. Direct smear: Strongyloides stercoralis rst-stage rhabditiform (L1) larvae (A). Close-up of the anterior end of S. stercoralis
larva showed a short buccal canal and the rhabditoid oesophagus (B).

respectively. In addition, IV metronidazole (Flagyl , Sano-
Aventis, Paris, France, 50 mg/kg/day) was administered to
treat intestinal bacterial overgrowth infection. At day three,
when oral via was restored, PO sucralfate (Ulcar ; Sano-
Aventis, Paris, France, 1 g/day) was administrated, followed
by PO fenbendazole (Panacur , Intervet, Angers, France,
50 mg/kg/day, during seven days) associated to IV metro-
nidazole, in order to treat intestinal strongyloidosis and
giardiosis. Finally, IV amoxicilline (Clamoxyl , Laboratoire
Glaxosmithkline, Marly-Le Roi, France, 20 mg/kg/day) was
used to treat B. bronchiseptica pulmonary infection. During
hospitalization, fresh faecal samples were daily collected
and analysed by direct smear and the Baermann method.
At day seven, both techniques scored negative for par-
asitic stages and the treatment with fenbendazole was
suspended. At the control day (day nine), a fresh faecal sam-
ple, analysed by direct smears, revealed alive S. stercoralis
larvae and a treatment with PO ivermectin (Ivomec ;
Merial, Lyon, France, 0,5 mg/kg/day, during seven days) was
promptly undertaken. Negativity to S. stercoralis infection
was achieved at day 14, ve days from the beginning of
the treatment with PO ivermectine. Fresh faecal samples
were analysed by Baermann method during 6 months after
treatment and all resulted negative for the presence of
parasites. However, loose stools were present until 30 days
after commencing therapy with ivermectin, requiring hyper-
digestible dietary treatment (Hypoallergenic , Royal Canin).
The treatment, clinical follow-up and results of faecal exam-
inations are summarized in Table 1.
Discussion
In dogs, infection by S. stercoralis is often moderate and
asymptomatic, with few cases showing apparent intestinal
signs [22]. However, severe disease and hyperinfection has
been observed in puppies and immunocompromised hosts,
which may display broncho-pneumonia, watery to mucous
diarrhoea and sudden death [1]. Conversely, in humans
the syndrome is mainly featured by gastrointestinal, cuta-
neous and pulmonary symptoms [23]. In dogs, iatrogenic
immunosuppressive status secondary to long corticosteroid
treatment has been considered as a potential factor asso-
ciated with severe hyperinfection forms [24]. Data here
reported suggest that the migration of a large number of
S. stercoralis larvae in the upper respiratory tract may have
caused broncho-alveolar pneumonia and local inammation,
resulting in the overgrowth of B. bronchiseptica. At the
mean time, intestinal S. stercoralis and G. duodenalis co-
infection and, secondary bacterial overgrowth, may explain
the persistence of diarrhoea observed in the dog [1]. The
presence of G. duodenalis in the digestive tract induce loss
of epithelial absorptive surface area through brush-border
retraction and increased rates of enterocyte apoptosis by
consuming local arginine [25]. Previous studies have estab-
lished that a combination of malabsorption and secretion of
electrolytes seems to be responsible for uid accumulation
in the intestinal lumen during Giardia infection, associated
to local arginine consumption by the parasite resulting in
loss of epithelial barrier function [26]. Remarkably, hyper
digestible diet, that is rich in arginine, should be adminis-
tered during giardiosis, in order to allow a rapid recovery
following the treatment of the infection.
Results from this study conrm that routine copromicro-
scopic methods may fail to diagnose S. stercoralis infection.
Indeed, even when present, larvae in faeces become eas-
ily altered and unrecognisable when saturated salt solutions
are added [1]. Specic parasitological skills and methods,
including fresh faecal smears and the Baermann technique,
are then required for detecting S. stercoralis larvae in vivo
[3], although the sensitivity of these methods may be low
when larval output is irregular [27].
Finally, although fenbendazole is considered the drug of
choice for the treatment of S. stercoralis infection in dogs

Please cite this article in press as: Cervone M, et al. Strongyloides stercoralis hyperinfection in an immunosuppressed
dog from France. Revue vtrinaire clinique (2016), http://dx.doi.org/10.1016/j.anicom.2016.05.001
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VETCLI-41; No. of Pages 5 ARTICLE IN PRESS
Strongyloides stercoralis hyperinfection in an immunosuppressed dog from France
[1,2], ivermectin may be a valid alternative [14]. Indeed,
in the dog here examined, the treatment with fenbenda-
zole (50 mg/kg/day, for seven consecutive days) was not
effective and the negativity of S. stercoralis infection was
gained only after inclusion of ivermectin (0.5 mg/kg/day, for
seven consecutive days) in medical protocol. This result may
indicate that in case of immunodeciency status, primitive,
iatrogenic or consequent to co-infection with other para-
sites, ivermectin may be necessary. However, this is a not
approved drug for the treatment of canine strongyloidosis
and low safety margins have been reported in some breeds.
In conclusion, the present report should aware veterin-
arians on the potential occurrence of natural S. stercoralis
hyperinfection cases in dogs. In France, the prevalence
of canine strongyloidosis is unknown and further studies
should be carried out to investigate the epidemiology of this
neglected and, as yet, little-known zoonotic parasite.
Disclosure of interest
The authors declare that they have no competing interest.
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