Equine pythiosis: Report of 28 cases from São Paulo State, Brazil Pitiose em equinos: Relato de 28 casos no estado de São Paulo, Brasil

Abstract

Pythiosis is a granulomatous lesion of the skin and subcutaneous tissues caused by Pythium insidiosum, a microorganism belonging to the Stramenopila Kingdom and the Oomycetes Class. The pathogen is commonly found in water environments, mainly in tropical areas of the world. Twenty eight cases of equine pythiosis were presented at the Large Animal Surgery Department of the School of Veterinary Medicine and Animal Science, São Paulo State University, Brazil in six years. Among the 28 animals, 13 presented distal lesions on the limbs, with four being immediately euthanized and seven dying due to loss of body condition leading to cachexia. The horses presented with one or more wounds in the body, distributed as follows: limbs (13 distal, four proximal), abdominal region (7), thoracic region (1), pectoral region (1), lumbar region (1), nasal region (1) and prepuce (1). The diagnosis was made by the association of the macroscopic aspects of the lesions with the histopathology, isolation of the pathogen and/or nested-PCR. Treatments included surgical removal of the lesion (16), potassium iodide 67 mg kg-1

Full text

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Semina: Ciências Agrárias, Londrina, v. 36, n. 2, p. 909-916, mar./abr. 2015
Recebido para publicação 20/05/14 Aprovado em 24/11/14
DOI: 10.5433/1679-0359.2015v36n2p909
Equine pythiosis: Report of 28 cases from São Paulo State, Brazil
Pitiose em equinos: Relato de 28 casos no estado de São Paulo,
Brasil
Marcos Jun Watanabe1; Juliana de Moura Alonso2; Ana Liz Garcia Alves1;
Ana Lúcia Miluzzi Yamada2; Sandra de Moraes Gimenes Bosco3;
Celso Antônio Rodrigues1; Carlos Alberto Hussni1*
Abstract
Pythiosis is a granulomatous lesion of the skin and subcutaneous tissues caused by Pythium insidiosum,
a microorganism belonging to the Stramenopila Kingdom and the Oomycetes Class. The pathogen is
commonly found in water environments, mainly in tropical areas of the world. Twenty eight cases of
equine pythiosis were presented at the Large Animal Surgery Department of the School of Veterinary
Medicine and Animal Science, São Paulo State University, Brazil in six years. Among the 28 animals,
13 presented distal lesions on the limbs, with four being immediately euthanized and seven dying due
to loss of body condition leading to cachexia. The horses presented with one or more wounds in the
body, distributed as follows: limbs (13 distal, four proximal), abdominal region (7), thoracic region (1),
pectoral region (1), lumbar region (1), nasal region (1) and prepuce (1). The diagnosis was made by the
association of the macroscopic aspects of the lesions with the histopathology, isolation of the pathogen
and/or nested-PCR. Treatments included surgical removal of the lesion (16), potassium iodide 67 mg kg-1
PO sid (23), intravenous regional perfusion with 50 mg of amphotericin B (6) and immunotherapy (8).
Pythiosis is a disease that develops quickly, but its diagnosis is time-consuming; therefore, establishing
an early treatment with special attention to the involvement of distal regions of the limbs is important.
Key words: Equine, granulomatous, pythiosis, Pythium insidiosum, surgery, wound
Resumo
A pitiose é uma doença granulomatosa do tecido cutâneo e subcutâneo causado pelo oomiceto Pythium
insidiosum, microorganismo pertencente ao reino Stramenopila, classe Oomycetes. O agente é
comumente encontrado em ambientes aquáticos, principalmente nas áreas tropicais do mundo. Foram
atendidos 28 casos no Serviço de Clínica Cirúrgica de Grandes Animais da Faculdade de Medicina
Veterinária e Zootecnia, UNESP, Botucatu, São Paulo, Brasil. Dentre os 28 animais, 13 apresentaram
lesões distais de membro, sendo quatro imediatamente submetidos à eutanásia e sete morreram devido
à perda progressiva de condição corporal levando a caquexia. Os equinos apresentaram uma ou mais
lesões, distribuídas da seguinte forma: membros (13 distais e quatro proximais), região abdominal (7),
região torácica (1), região peitoral (1), região lombar (1), região nasal (1), prepúcio (1). O diagnóstico
foi baseado na associação dos achados macroscópicos, histopatológicos, isolamento do patógeno e/ou
nested-PCR. Os tratamentos incluíram: remoção cirúrgica (16), iodeto de potássio 67 mg kg-1 VO Sid
(23), perfusão regional com 50 mg de anfotericina B (6) e imunoterapia (8). A pitiose é uma doença
1 Profs., Faculdade de Medicina Veterinária e Zootecnia, FMVZ, Botucatu, SP, Brasil. E-mail: watanabe@fmvz.unesp.br;
anaalves@fmvz.unesp.br; rodriguesca@fmvz.unesp.br; cahussni@fmvz.unesp.br
2 Discentes, FMVZ, Botucatu, SP, Brasil. E-mail: juliana.alonso@fmvz.unesp.br; anayamada@fmvz.unesp.br
3 Profª, Instituto de Biociências de Botucatu, IBB, Botucatu, SP, Brasil. E-mail: smgbosco@ibb.unesp.br
* Author for correspondence

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Watanabe, M. J. et al.
de rápido desenvolvimento, sendo imprescindível o diagnóstico rápido com especial atenção às lesões
localizadas na região distal do membro.
Palavras-chave: Cirurgia, equinos, feridas, granuloma, Pythium insidiosum, pitiose
Introduction
Pythiosis is a potentially life-threatening
disease of mammals and man, characterized by
granulomatous, exudative and itchy lesions of
cutaneous and subcutaneous tissues. It is caused
by the organism called Pythium insidiosum, an
oomycete belonging to the Kingdom Stremenopila,
Phylum Oomycota, Class Oomycetes, Family
Pythiaceae. The disease occurs predominantly in
tropical and subtropical areas and has been reported
mainly in the Americas and Southeastern Asia
(GAASTRA et al., 2010; SALLIS et al., 2003).
The genus Pythium comprises phytopathogenic
species, and the most common species to cause
disease in animals is P. insidiosum, although P.
aphanidermatum, a species that occasionally
causes disease in humans, has been identied
recently (CALVANO et al., 2011). The organism
lives in aquatic environments with the presence
of vegetation, and thus pythiosis is also known as
“swamp cancer” (AUSTWICK; COPLAND, 1974).
In Brazil, the disease occurs predominantly in
horses and dogs, and outbreaks of pythiosis have
been reported in sheep and in cattle (CARRERA et
al., 2013; GABRIEL et al., 2008; TORRES NETO
et al., 2010; SANTOS et al., 2011a). There has been
only one case reported of human pythiosis in Brazil.
The patient acquired the disease in a lake whilst
shing in standing water (BOSCO et al., 2005;
MARQUES et al., 2006). The disease also occurs
in cats, but it has not yet been reported in Brazil
(GAASTRA et al., 2010).
Due to its afnity with water environments and
vegetation, the life cycle of this organism comprises
the formation of sporangium at the tip of hyphae
that grows on grasses. Inside the sporangium, the
protoplasmatic material owing from the hyphae
is cleaved and matures to form zoospores. Once
maturated, these biagelated zoospores are released
into the water and swim around for 10-15 minutes
until encystation in plant material or damaged
mammalian skin. Once they penetrate the skin,
the zoospores lose their agella, and a germinative
tube develops to initiate hyphae growth, which is
the invasive form of the pathogen. The optimal
temperature for its growth is approximately 30-
40 °C, similar to mammalian body temperatures
(KRAJAEJUN et al., 2010).
The macroscopic characteristics of the lesion
in horses are the exuberant granulomatous tissue,
which develops within few weeks, and drainage of
serosanguineous to pyogenic exudates. The marked
characteristic of equine pythiosis is the formation of
“kunkers”, which correspond to small granulomas
containing hyphae surrounded by eosinophils
(KRAJAEJUN et al., 2010). Pruritis is intense and
leads to self-mutilation of the lesion in an attempt
to relieve the discomfort (GAASTRA et al., 2010).
Treatment of equine pythiosis consists of surgical
removal, administration of antifungal drugs, such
as amphotericin B and iodide compounds, and
immunotherapy (DÓRIA et al., 2012; GAASTRA
et al., 2010).
Cases presentation
A total of 28 horses (11 geldings and 17 mares),
aged 3-21 years old and of different breeds, were
attended at the Hospital of the School of Veterinary
Medicine and Animal Science at UNESP/Botucatu,
Brazil, between 2007-2012. These horses came
from different regions of São Paulo State, and had
free access to natural reservoirs of water or swamp
areas with high environmental temperatures.

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Equine pythiosis: Report of 28 cases from São Paulo State, Brazil
Clinical ndings
The lesions presented in different locations and
sizes, with 17 presenting wounds on their limbs
(four in the proximal limb and 13 in the distal limb),
seven on their abdomen, and the remainder with
single lesions over the chest, esternum, lumbar,
nostril and prepuce regions (Table 1). One of the
horses presented two lesions (abdominal and
proximal limb). All patients presented with intense
pruritis and the wounds have been rubbed against
objects or self-mutilated by bites; thus, blood and
secretions around the lips and bleeding wounds were
commonly observed. The granulomatous lesions
presented with ulceration and irregular aspects,
containing exudates ranging from serosanguineous
to mucopurulent. Fistulous tracts, focal necrosis
and characteristic foul odors were also observed,
in addition to the presence of yellowish masses
(“kunkers”).
Table 1. Distribution of cases, gender, lesion location, treatment and outcome of horses affected by pythiosis.
Case GenderaSite of lesion Treatment Outcome
1 M Spine KIbRemission
2 G Chest KI/ Immunotherapy Remission
3 G Prepuce Surgery/KI Death
4 G Nostril Surgery/KI Remission
5 M Sternum Surgery/KI/Immunotherapy Remission
6 M Abdomen KI Remission
7 M Abdomen Surgery/KI Remission
8 G Abdomen Immunotherapy Remission
9 M Abdomen KI Remission
10 G Abdomen Surgery/KI Remission
11 M Abdomen and olecranon Surgery/KI Remission
12 M Abdomen KI Remission
13 M Semitendinosus muscle Surgery/KI/Immunotherapy Remission
14 G Semitendinosus muscle Surgery/KI Remission
15 G Semimembranosus muscle Surgery/KI Remission
16 M Metacarpophalangeal joint KI/Immunotherapy Remission
17 M Carpus KI/ Amphotericin B/ Immunotherapy Death
18 G Metacarpophalangeal joint Surgery/KI Death
19 M Metacarpophalangeal joint None Euthanasia
20 M Metacarpophalangeal joint Surgery/KI/Amphotericin B/Immunotherapy Death
21 G Metacarpophalangeal joint Surgery/KI/Amphotericin B Death
22 M Metacarpophalangeal joint Surgery/KI/Amphotericin B Remission
23 M Metacarpophalangeal joint Surgery/KI/Amphotericin B Death
24 G Metacarpophalangeal joint None Euthanasia
25 M Metacarpal Surgery/KI/Amphotericin B Death
26 M Metacarpophalangeal joint KI Death
27 M Metacarpophalangeal joint None Euthanasia
28 G Metacarpal None Euthanasia
a Gelding (G) and Mare (M). b Potassium iodide (KI).
Potassium iodide dose = 67 mg kg-1 VO SID; Amphotericin B dose = 50 mg/animal.

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Horses that showed wounds on their limbs
presented with varying degrees of lameness due
to the structures compromised by the lesion.
Animals that exhibited intense lameness and deep
wounds presented periosteal proliferations, which
were observed by radiographic and post mortem
examinations.
Diagnosis
This was based on the gross lesions,
histopathology and identication of the pathogen
or nested-PCR with specic primers, as proposed
by Grooters and Gee (2002). Concerning the
macroscopic aspects, the granulomatous and
ulcerative pattern, observation of pruritis, presence
of serosanguineous to mucopurulent exudates and
presence of stulous tracts with kunkers were
considered.
The histopathology revealed suppurative and
granulomatous inammation characterized by
hyphae surrounded with degranulated eosinophils
and collagen. The hyphae margins contained intact
eosinophils and neutrophils, which composed an
inammatory exudate.
The culturing of P. insidiosum was performed
with several washes of freshly removed kunkers
from the lesions with saline and chloramphenicol
(50 µg mL-1). The kunkers were sliced and plated on
Sabouraud Dextrose Agar (SAB) 4 % and incubated
at 35 °C for 24 hours, which was enough time to
observe the hyphal growth of the pathogen. When
culturing was not possible, DNA extraction from
the kunkers was performed, and nested-PCR was
employed to conrm the molecular identity of the
pathogen.
Treatment
The principal treatment was surgery to
completely or partially remove the lesion combined
with potassium iodide (Vetec® - Sigma Aldrich Co)
(67 mg kg-1, SID) for 45 - 60 days. This protocol
was used in 16 cases, and some of them required
repeated surgical approach (Table 1). Among the
cases presented, all horses with lesions not located
in the distal limb achieved total remission of the
lesions, with exception of the horse which lesion
was in the prepuce that died because a colic episode
not related with pythiosis. However, of 13 horses
with lesions in the distal region of the limbs, only
two were cured. These animals presented recent
lesions and one of them was also submitted to
amphotericin B treatment. Potassium iodide not
associated with surgery was used in 8 cases where
surgical debridement was not possible or necessary.
The horses that showed lesions in the distal
regions of their limbs and had no improvement
with potassium iodide were submitted to treatment
with amphotericin B and/or immunotherapy.
Amphotericin B (Funtex® - Meizler Biopharma S/A,
São Paulo, Brazil ), 50 mg/animal, was administered
by intravenous regional perfusion after a tourniquet
was applied above the lesion. After 40 minutes, the
circulation was slowly released. This approach was
employed in six animals and repeated after 14 days
if necessary, according to the progression of the
lesion (Table 1).
Immunotherapy with Pithium Vac® (Lapemi/
Embrapa, Santa Maria, Rio Grande do Sul, Brazil)
was performed in seven animals by the subcutaneous
route in the neck region every 14 days, according
to the manufacturer’s instructions. In the majority
of cases, three to ve applications were necessary
(Table 1). An efcacy of 71.4 % was observed
among the horses treated with immunotherapy.
Only one animal was treated exclusively with
immunotherapy, with the remaining treated in
conjunction with surgery and/or potassium iodide
(Table 1).
The treatment choice was based on the
assessment of the possibility of surgical excision
and on lesion extension. The standard treatment
was the association of surgical excision and
potassium iodide. In the absence of excision

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Equine pythiosis: Report of 28 cases from São Paulo State, Brazil
possibility and/or responsiveness to therapy, other
therapeutic possibilities were added. The addition
of immunotherapy was enlightened to the owner,
and added or not to the treatment depending on the
extent of injury and the owner nancial condition.
Outcomes
Among the 28 animals evaluated, those
considered cured were those with lesions found
in proximal regions of their limbs and abdominal,
nasal, chest, lumbar and esternum regions. Among
the 13 animals that presented lesions in the distal
regions of their limbs, four were euthanized
immediately, seven died due to the progressive loss
of their body condition leading to cachexia, and
only two were cured (Table 1). The animal with a
lesion in the prepuce died during the treatment due
to colic not related to pythiosis.
Euthanasia decision was based on the extent and
depth of injury associated with prolonged evolution,
lameness, weakness and cachexia.
Post mortem ndings
The post mortem descriptions by the pathologists
corroborate the macroscopic ndings of the lesions.
Systemic involvement was not observed. In two
of the euthanized animals, which had a disease
duration greater than 90 days, the penetration of
the pathogen into the bone tissue with resulting
periosteal proliferation was observed.
Discussion
The 28 cases herein reported occurred during
the last seven years, with 23 occurring in the last
three years. This incidence demonstrates the great
importance of this disease, which has become
emergent. We observed that these cases occurred
after rainy periods, especially in swampy areas with
great hydric efuents, which has been previously
demonstrated in the literature (LEAL et al., 2001).
The macroscopic aspects of the wounds were
in accordance with the previous literature, which
has reported a high occurrence of unique lesions,
although multifocal lesions have been described
(GAASTRA et al., 2010; LEAL et al., 2001;
MOSBAH et al., 2012). The lesions on the limbs
are common (SALLIS et al., 2003) and evolved
quickly with great exudation due to the amplitude of
the wounds and constant loss of the body condition,
with anemia and hypoproteinemia as consequences
of intense blood discharge observed in the lesions.
The evaluated animals that presented extensive
wounds on their limbs that reached deep structures
showed lameness of several degrees, especially
if the lesions affected the periosteal regions. No
systemic disease was observed among the animals
that died or had to be euthanized, corroborating
the literature that highlights the high incidence of
cutaneous lesions in equine pythiosis (GAASTRA
et al., 2010; LEAL et al., 2001; MOSBAH et al.,
2012).
Pythiosis is diagnosed by the association of the
macroscopic aspects of the lesion, histopathology,
cytology, immunohistochemistry, serology, culture
and, recently, molecular approaches. Histopathology
and cytology do not differentiate between the
hyphae from P. insidiosum and zygomycetes
fungi (GAASTRA et al., 2010, SANTURIO et al.,
2006b). Its early diagnosis is difcult as several
differential diagnoses can be considered, such as
cutaneous habronemosis, neoplasia, exuberant
granulomatous tissue and fungal and bacterial
granulomas (GAASTRA et al., 2010; LEAL et al.,
2001; WHITE, 2005).
Treatment is difcult because an early denitive
diagnosis is seldom made. The pathogen does not
respond satisfactorily to antifungal compounds,
although they are widely employed in its treatment.
P. insidiosum lacks ergosterol in its cellular
membrane, the main target of azoles, allylamines
and polyenes. The treatment of choice is surgical
removal of the entire lesion, which is not always
feasible due to the unclear anatomic localization

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Watanabe, M. J. et al.
of the lesions, especially in the limbs (LEAL et al.,
2001; SANTURIO et al., 2006a). The combined
administration of antifungal compounds, iodide
(such as potassium and sodium iodide) and
immunotherapy is common (GAASTRA et al.,
2010; SANTURIO et al., 2006a).
According to Chafn et al. (1992), the
combination of potassium iodide with surgery
allowed better results for the treatment of equine
pythiosis. In the present report, some animals
with lesions in the distal parts of the limbs did not
respond well to the combination of surgery and
potassium iodide, leading to other therapies, such as
amphotericin B and immunotherapy.
Amphotericin B is an antimycotic agent from the
polyene group with an efcacy reported to be 92
% in conjunction with surgery and thermocautery
(DÓRIA et al., 2012). In the present study, only one
animal had total remission of the lesion with such
an approach.
The immunotherapy success rates varied
from 50-83.3 % (MENDOZA et al., 1986, 1992;
SANTOS et al., 2011b) and when in association
with surgery these rates increases to 90% (SANTOS
et al., 2011b). In the present study, a similar rate
described by Santos et al. (2011b) was observed
(71.4%), however this rate was achieved with
immunotherapy alone and/or associated with
surgery and/or potassium iodide.
It is important to emphasize that the most
effective treatments were surgical removal of
the lesion combined with potassium iodide and
immunotherapy. However, independent of the
treatment adopted, when lesions were found in
the distal part of the limbs, the prognosis was
unfavorable as 11 out of 13 animals with lesions in
the distal part of the limbs died.
The low rate of remission presented in distal
limb rests on the fact that the equine species
has peculiarities such as chronic inammation,
exuberant development of granulation, slow
epithelialization and inefcient contraction
(THEORET; WILMINK, 2008). The healing
difculty in distal limb can also be attributed to
anatomical and physiological characteristics of this
region, which includes smaller blood supply, joint
high mobility, higher level of contamination due
to proximity to the ground and no muscle support
(HENDRICKSON, 2005). Possibly, the lack of
muscle support facilitated the Pythium inltration
to structures such as tendons, ligaments and bones,
which resulted in a worse prognosis.
Conclusion
The horses that had total remission of the lesions
were the ones submitted to early and aggressive
treatment. The success of the treatment depends on
the length of the morbidity, the location and size of
the lesion. The involvement of deep structures did
not allow surgery excision and led to an unfavorable
prognosis, with euthanasia being recommended.
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