Download Micobacterioses em animais selvagens. Mycobacterial

RCPV (2013) 108 (587-588) 113-119
Micobacterioses em animais selvagens.
Mycobacterial diseases in wild animals.
Filipa F. Loureiro1*, Joana Valente2, Roberto Sargo2, Manuela M. Matos3, Ana C. Coelho4
1
Department of Veterinary Sciences, University of Trás-os-Montes and Alto Douro (UTAD), 5001-801 Vila Real, Portugal
Centre for Recovery of Wild Animals (CRAS) – Veterinary Hospital of University of Trás-os-Montes and Alto Douro (UTAD),
5001-801 Vila Real, Portugal
3
Department of Genetics and Biotechnology, Institute of Biotechnology and Bioengineering, Centre of Genomic and Biotechnology, University of Trás-os-Montes and Alto Douro (UTAD), 5001-801 Vila Real, Portugal
4
Veterinary Microbiology Laboratory, Veterinary Medicine, Department of Veterinary Sciences, CECAV, University of Trás-os-Montes and
Alto Douro (UTAD), 5001-801 Vila Real, Portugal
2
Resumo: A tuberculose aviária é uma doença infeciosa de carácter crónico e desenvolvimento insidioso, que muitas vezes
apresenta um desfecho fatal. Devido ao seu potencial zoonótico
assume um importante papel na saúde pública. O diagnóstico
em animais vivos mantém-se difícil de obter, destacando-se a
biologia molecular como uma alternativa rápida e específica,
comparativamente aos outros métodos diagnósticos disponíveis.
O objetivo desta revisão foi compilar informação sobre os principais agentes etiológicos responsáveis por provocar a infeção
em fauna selvagem, bem como os dados epidemiológicos conhecidos, de forma a prestar apoio a médicos veterinários, alunos,
técnicos e investigadores da área.
Palavras-chave: tuberculose aviária; fauna selvagem; Mycobacterium; biologia molecular.
Summary: Avian tuberculosis is a chronic infectious disease
with an insidious development, which often presents a deadly
outcome. Because of its zoonotic potential, it takes on an important role to public health. The diagnosis in living animals is
still hard to get, and molecular biology stands out as a quick and
specific alternative, when compared to other available means of
diagnosis. The aim of this revision was to compile information
on the main etiologic agents responsible for causing the infection in wild animals, as well as the known epidemiologic data,
so as to give support to veterinaries, students, technicians and
researchers in the area.
Keywords: avian tuberculosis; wildlife; Mycobacterium; molecular biology.
Introduction
The genus Mycobacterium is a group of intracellular bacteria, Gram-positive, with a cell wall rich in
lipids and hydrophobic, highly resistant to desiccation, ultraviolet light and freezing (Converse, 2007).
*Correspondência: [email protected]
Tel: +351 259350405; Fax: +351 259350629
The mycobacteria are divided into groups according
to some criteria: pathogenicity to animals or humans,
growth rate and optimum temperatures, and effect of
visible light on pigment production (for example, M.
avium produce yellow pigment on the absence of light)
(Inderlied et al., 1993).
The genus Mycobacterium includes pathogenic
species for many animals: birds (M. avium), mammals
(M. avium subsp. paratuberculosis, M. bovis, M. tuberculosis), fishes (M. marinum), frogs (M. fortuitum) and
rodents (M. lepraemurium) (Converse, 2007).
Tuberculosis, caused by M. tuberculosis (MTC),
was considered the “typical” mycobacteriosis, thus
making all other, except M. leprae, being described
as “atypical” (Inderlied et al., 1993; Cangelosi et al.,
2004).
Mycobacterium avium complex
Avian mycobacteriosis presents ubiquitous distribution, and is described in wild and captive birds all
over the world (Converse, 2007). It’s caused by Mycobacterium avium serotypes 1-3, less frequently by Mycobacterium genavense (Mijs et al., 2002) and rarely
by M. intracellulare, M. fortuitum, M. tuberculosis,
M. gordonae and M. nonchromogenicum (Kunze et
al., 1992; Dvorska et al., 2004, M. genavense’s detection has increased in captive birds, instead of M. avium
(Pollock, 2006; Converse, 2007). Sporadically, other
potentially pathogenic mycobacteria are found in bird
tissues, e.g. M. celatum, M. simiae and M. chelonae
(Moravkova et al., 2011).
Although the term mycobacteriosis can be applied
to any infection of mycobacteria, the term avian tuberculosis is more used for the disease caused by M.
avium or related agents, due to its typical tuberculous
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Loureiro F. et al.
lesions (Converse, 2007). The agent M. tuberculosis is
occasionally found in birds, but its clinical signs are
different (Kearns, 2003).
Avian tuberculosis is a chronic disease, with a long
incubation period depending on the physical health of
the bird and virulence of the strain of M. avium avium
(Moravkova et al., 2011), that leads to anorexia, lethargy, emaciation and dyspnea; death can occur in a few
months. The agent can persist in the environment and
populations during years. It has been verified a high
incidence of avian tuberculosis in captive populations,
with high number of birds in a contaminated area
(Converse, 2007).
Avian tuberculosis is still difficult to diagnose and
control in living birds (Kearns, 2003). There are no reports of birds species that are resistant to all mycobacteria (Converse, 2007).
The agents that are included in M. avium complex
(MAC) are opportunistic microorganisms, able to
cause disease in humans and animals (Inderlied et al.,
1993), and are subdivided in four subspecies: M. avium
subsp. avium, M. avium subsp. silvaticum, M. avium
subsp. homnissuis e M. avium subsp. paratuberculosis
(Converse, 2007). M. avium is an important pathogen
for humans and animals (Bono et al., 1995). MAC’s
microorganisms were responsible for an opportunistic
infection in 70% of the people with Acquired Immunodeficiency Syndrome (AIDS) in developed countries
before the appearance of modern anti-retroviral drugs
(Cromie et al., 2000). M. avium’ serotypes 1, 2 and
3 are the most frequently isolated from animals; serotypes 4-8 are the most often involved in immuno compromised individuals (Kunze et al., 1992).
Mycobacterium avium subsp. avium affects mainly
birds, despite being documented also in bovines and
pigs (Moravkova et al., 2008). Most of birds’ infections are caused by serotypes 1-3 of M. avium (Cromie
et al., 2000). M. avium subsp. homnissuis (serotypes
4-6, 8-11 and 21) is an opportunistic agent, mainly infectious to immunocompromised humans, pigs, cattle
and cervids (Dvorska et al., 2004). M. avium subsp.
silvaticum is documented only in wood pigeons (Columba palumbus). M. avium subsp. paratuberculosis is
the causative agent of paratuberculosis (Johne’s Disease), a chronic inflammation of gastrointestinal tract,
that mainly affects ruminants (Moravkova et al., 2008;
Castellanos et al., 2012), despite having a large spectrum of hosts (Motiwala et al., 2004). Paratuberculosis
is described in many wild species, such as the roe deer
(Capreolus capreolus), the European rabbit (Oryctolagus cuniculus) and the red fox (Vulpes vulpes) (Greig
et al., 1999; Carta et al., 2012). A recent study written by Carta et al. revealed that the red deer (Cervus
elaphus) doesn’t contribute, as a reservoir, to maintain
M. avium subsp. paratuberculosis on the Iberian Peninsula. On the other hand, that study refers the high
prevalence of M. avium subsp. paratuberculosis in
the fallow deer (Dama dama) in the same geographic
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RCPV (2013) 108 (587-588) 113-119
area (Carta et al., 2012). In some predator carnivores,
the same agent was isolated 6 times more than it was
in preys (Castellanos et al., 2012). The association of
paratuberculosis with the Crohn’s Disease in humans
is still being studied (Greig et al., 1999; Motiwala et
al., 2004; Rodríguez-Lázaro et al., 2005; Castellanos
et al., 2012).
Eventually, M. avium can cause mycobacteriosis
in all bird species, but it affects mainly the waterfowl,
Galliformes, Columbiformes, Passerines, Psitaccines,
ratites and raptors (Aranaz et al., 1997; Pollock, 2010).
Epidemiology
Mycobacteria are opportunistic microorganisms
that live under various temperatures and pH conditions,
in damp environments (Cromie et al., 2000; Converse,
2007). Avian tuberculosis is primarily transmitted by
direct and indirect contact with infected birds by M.
avium (Converse, 2007). Raptors can be infected by
ingestion of contaminated preys (Pollock, 2006). Mycobacteria can also be dispersed as aerosols, in case of
animals with respiratory signs. The environment can
persist contaminated for a long period of time. Liver
and intestinal granulomas continuously liberate bacillus to fecal material. M. avium can persist outside the
animal host, producing mycobactin and acquiring iron,
essential to his growth and survival in the environment
(Converse, 2007).
The most important infection routes are the respiratory and gastrointestinal tracts (bronchial and intestinal
mucosa, respectively) (Inderlied et al., 1993). There is
evidence that M. avium can be transmitted mechanically, by arthropods (Converse, 2007). Some mycobacteria have been isolated from coleopterans (Fischer et
al., 2004). In case of paratuberculosis, M. avium subsp.
paratuberculosis, it is mainly transmitted by feco-oral
route, through colostrum, milk or contaminated pasture, but it can also be transmitted by other routes, such
as intravenous, intramammary and intrauterine (Castellanos et al., 2012).
Susceptibility to mycobacterial infections depends
on different factors, both genetic and environmental
(Aranaz et al., 1997; Converse, 2007). Apparently, M.
avium subsp. avium infection makes the infection with
concurrent less virulent mycobacterial species easier
(Moravkova et al., 2011).
The agents of avian mycobacteriosis in pet birds
are rarely identified, due to lack of specific findings
at necropsy and difficulties in isolating mycobacterial
species (Manarolla et al., 2009).
Avian tuberculosis is more frequently diagnosed in
adult birds, between 3 and 10 years of age (Pollock,
2010). The diagnosis in birds with less than 2 years old
it’s very rare (Soler et al., 2009).
Incidence and prevalence of avian tuberculosis
remain unknown, due to the lack of specific clinical
Loureiro F. et al.
symptoms and accurate diagnostic tests (Moravkova
et al., 2011). It’s influenced by species, age, housing
conditions and if birds are in wildlife or captive (Soler
et al., 2009). According to data on macroscopic findings at necropsies of wild birds, the prevalence of avian
tuberculosis is estimated to be at least 1% (Moravkova
et al., 2011).
Clinical signs
The most common clinical signs are: anorexia,
progressive weight loss, weakness, feather damages,
diarrhea, abdominal distension, lethargy and death. In
case of pulmonary, ocular or bone involvement, dyspnea, blindness and lameness can occur (Converse,
2007).
Granulomatous lesions are common in raptors,
but rare in Anseriformes, Columbiformes, Coracciformes, Passeriformes and Psittaciformes. The diffuse form of disease was mainly described in Coracciformes (Alcedo spp.) and Passeriformes (Pollock,
2006).
Infections by M. avium and M. genavense produce
very similar clinical signs in birds (Converse, 2007).
In veterinary epidemiology, the virulent strains that
induce avian tuberculosis are the most important ones
(Pavlik et al., 2000).
Paratuberculosis, an intestinal granulomatous
disease, is characterized by emaciation, at first with
an increased appetite and after with anorexia, lethargy and chronic or intermittent diarrhea. Abdominal
distension can occur due to hepatomegalia or small
intestines enlargement. Musculoskeletal disease on
avian tuberculosis is described with various incidences, being the carpometacarpal and elbow joints
the most commonly involved. Skin above the affected
places appears thickened and ulcerated. Respiratory
form of disease results in dyspnea and exercise intolerance, due to pulmonary granulomas and/or air sacs
compression, secondary to enlargement of the liver.
Nodules within the infraorbital sinus, nares and syrinx are rare, despite being described. Skin disease,
also rare, involves dermatitis, non pruritic thickening,
xantomatosis and soft subcutaneous masses (Pollock,
2006).
In humans, M. avium infection results in one of
the following presentations: 1) primary localized lymphadenitis, 2) pulmonary disease or 3) generalized
disease, associated to immunossupression (Aranaz et
al., 1997). The serotypes 1, 4 and 8 are the most commonly responsible for the mycobacteriosis associated
to AIDS (Aranaz et al., 1997).
Mammals’ immune response to M. avium includes
leucocytes, such as macrophages and T lymphocites,
particularly citotoxic T-cells and natural killer cells,
and citocines (TNF, IFN- γ, IL-2). Chikens’ response
appears to be similar (Cromie et al., 2000).
RCPV (2013) 108 (587-588) 113-119
Prevalence of mycobacteria in wild animals
in Portugal
In Portugal, the epidemiology of M. bovis in wild
boar (Sus scrofa) was described by Santos et al. (2009).
In this study, in the total of mycobacterial isolates, 43%
were M. bovis, 19,5% were M. avium and 36.6% were
other mycobacteria. In the same study the isolation
rates for M. bovis were 6%, 22%, and 46% in tuberculosis-infected areas.
In the Iberian Peninsula, paratuberculosis is uncommon in red deer (Cervus elaphus) and roe deer
(Capreolus capreolus). However, in the same area
a high Map infection prevalence among fallow deer
(Dama dama) was detected (Carta et al., 2012).
As far as we know, prevalence of avian tuberculosis
in wildlife is not well described in Portugal, yet.
Impact on wildlife populations
Tuberculosis is considered an emerging infectious
disease among wildlife, and is already described in
a wide number of wild species. Once established, it
is extremely difficult to eradicate. The only successful case of eradication was in Australia, with the depopulation of water buffalo (Bubalus bubalis), the
maintenance host of the infectious agent, M. bovis
(Santos et al., 2009). Tuberculosis is not a dangerous
threat to most wild carnivore populations, although it
could have a devastating effect in small populations,
like the Iberian linx (Linx pardinus) (Briones et al.,
2000). Several wild mammal species are involved in
the transmission and maintenance of M. bovis infection, such as Eurasian badgers (Meles meles) in Great
Britain, white-tailed deer (Odoicoleus virginianus) in
the United States and wild boar (Sus scrofa) in Spain
(Lyashchenko et al., 2008).
Avian tuberculosis occurs sporadically in wild
birds. The prevalence of the disease may be underestimated, because many carcasses remain undetected in
the wilderness or are removed by predators or hunters.
Bacterial infections are diagnosed, sometimes, when
epizootic episodes of other diseases happen, causing
high mortality (such as avian cholera).
Avian tuberculosis (M. avium serovar 1) is described as the cause of high mortality in lesser flamingos (Phoenicopterus minor) (Kock et al., 1999). The
potential of disease transmission increases in gregarious species; predators, whose diet is sick birds, are
also susceptible to higher risk (Converse, 2007). It’s
relatively rare in non-gregarious species, such as some
raptors (Tell et al., 2004).
Free-ranging raptors assume an important role on
mycobacteria dispersion (Soler et al., 2009). However,
they are not, apparently, a relevant source of infection
to captive birds (Pollock, 2006). Mycobacterium avium Complex (MAC) species also have been isolated
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Loureiro F. et al.
RCPV (2013) 108 (587-588) 113-119
in wild and domestic mammals (cattle and pigs) (Bartos et al., 2006). Prevalence of M. tuberculosis is described in wild boar (Sus scrofa) and red deer (Cervus
elaphus), potential reservoirs of bovine tuberculosis
(Vicente et al., 2006). Bovine tuberculosis is reported
in many wildlife species and countries (Martín-Atance
et al., 2005). The identification of reservoirs is crucial
to the implementation of effective controlling measures (Naranjo et al., 2008).
Mycobacterial diseases in wild animals
The most significant mycobacterial diseases of
free-living, captive and farmed deer are bovine tuberculosis (M. bovis), paratuberculosis (M. avium subsp.
paratuberculosis) and avian tuberculosis (M. avium
subsp. avium) (Mackintosh et al., 2004).
The reported prevalence, by some countries, of M.
bovis infection in wild deer doesn’t reach the 5%, except
in New Zealand, where the main suspect cause for such
a high level of infection is the spread from other wildlife
(Mackintosh et al., 2004). In Great Britain, the badger
(Meles meles) is the main wildlife reservoir of bovine
tuberculosis. The transmission between cattle, badgers
and deer has been proved, but the direction of spread has
not been disclosed. In Spain, the transmission between
cattle, deer and wild boar is reported, and tuberculosis
caused by M. bovis has been a major problem in collections of wildlife (Mackintosh et al., 2004).
The gross lesions of disease in deer tend to be similar to those found in cattle (Table 1). However, in deer
there are more abscesses containing liquid pus, rich in
bacillus, fewer calcification and without fibrosis. The
lymph nodes of the head are infected in almost half
of the cases, with caseous necrotic lesions. Infections
with M. avium subsp. paratuberculosis and M. avium
subsp. avium cause identical lesions to those caused by
M. bovis (Mackintosh et al., 2004).
Diagnosis
Ante mortem diagnosis is very difficult to obtain
(Tell et al., 2004). Avian tuberculosis must be considered as a differential diagnosis when adult raptors are
found unhealthy, weak and in poor condition without
any apparent reason. The probability increases if ce-
lomic abnormalities are detected during physical examination or diagnostic exams (Tell et al., 2004; Pollock, 2006). Granulomatous lesions in birds don’t tend
to calcify, as they do in mammals, what results in a
more difficult radiographic diagnosis (Pollock, 2006).
Minimum database analysis can reveal variable results.
However, a complete blood count might reveal a marked
heterophilic leukocytosis, monocytosis, thrombocytosis and biochemistry might reveal elevated fibrinogen,
as well as a polyclonal gammaglobulinopathy (Pollock,
2006). The most useful ante mortem diagnostic tests are
radiography, ultrasonography, laparoscopy and biopsy
or fine-needle aspiration with acid-fast staining. However, definitive diagnosis requires mycobacterial culture
or PCR test (Tell et al., 2004). Serologic tests EnzymeLinked Immunoabsorbent Assay (ELISA), complement
fixation and hemagglutination are available for only a
little number of species (Pollock, 2006).
Mycobacterium avium isolation or its amplification
in clinical samples doesn’t necessarily mean active infection, because M. avium is a common agent in the
environment and might be present in cases of absent
disease (Aranaz et al., 1997).
Post mortem diagnosis of avian tuberculosis is
based on the presence of typical lesions and mycobacterial detection on blood or tissues. Caseous
granulomas or other inflammatory lesions along the
intestine, liver, spleen, lungs, bone marrow, gonads
or kidneys can be found in post mortem examination
(Cromie et al., 2000; Converse, 2007; Moravkova et
al., 2011). A presumptive diagnosis is supported by
microscopic findings of acid-fast bacillus, if at least
5x104 mycobacteria/ml of material are present (Aranaz
et al., 1997; Converse, 2007). Mycobacterial culture
is difficult and delayed (might require a minimum of
4 weeks) (Converse, 2007). Isolation process includes
3 steps: enrichment, decontamination and prolonged
incubation (Coelho et al., 2007). Some media can be
used to MAC’s culture, but the most sensible method
requires, at least, culture in 2 media, 1 solid and 1 liquid. Multiple combination of culture media results in
higher sensitivity (Inderlied et al., 1993; Aranaz et al.,
1997). Several methods can be used to culture MAC
from blood, bone marrow or other specimens (Inderlied et al., 1993). Most mycobacterial strains can be
cultivated on the Löwenstein-Jensen medium at 28ºC
and 37ºC. Culture of Map has good results on Middle-
Table 1 – M. intracellulare and MAC microorganisms’ ability to produce macroscopic lesions in determinate species (adapted from
Mackintosh et al., 2004).
Animal species
M. avium subsp.
avium
M. avium subsp.
homnissuis
116
M. avium subsp.
silvaticum
M. avium subsp.
paratuberculosis
M. intracellulare
Deer
yes
rarely
yes
yes
unknown
Cattle
yes
rarely
unknown
yes
unknown
Pigs
yes
yes
unknown
rarely
probably
Humans
rarely
yes
unknown
rarely
rarely
Loureiro F. et al.
RCPV (2013) 108 (587-588) 113-119
Table 2 – Serotypes and DNA insertion sequences of the agents of the Mycobacterium avium complex (MAC) and M. intracellulare
(adapted from Mackintosh et al., 2004).
Characteristic
M. avium subsp.
avium
M. avium subsp.
homnissuis
M. avium subsp.
Silvaticum
M. avium subsp.
paratuberculosis
M. intracellulare
Serotypes
1, 2, 3
4-6, 8-11, 21
2, 3
-
7, 12-20, 25
IS900
no
no
no
yes
no
IS901/IS902
yes
no
yes
no
no
IS1245
yes
yes
yes
no
no
IS1311
yes
yes
yes
yes
yes
brook-Cohn 7H10 agar with OADC and mycobactin
enrichment (Harmsen et al., 2003). The culture on a
liquid medium can be done in a modified Middlebrook
7H9 liquid medium containing radioactively labelled
palmitic acid (BACTEC TB System; Becton-Dickinson Diagnostic Instrument Systems, Sparks, Md.) (Inderlied et al., 1993).
Molecular diagnosis provides a helpful and quick
alternative to biochemical test profiles of pure cultures
(Harmsen et al., 2003). Polymerase Chain Reaction
(PCR) based techniques need a small amount of sample to obtain results, detect a reduced number of microorganisms, give results in a short period of time and
might distinguish mycobacterial species (Aranaz et al.,
1997; Cangelosi et al., 2004; Coelho et al., 2007). Application of PCR to detect mycobacterial genome is
valuable for laboratory confirmation of the infectious
disease (Coelho et al., 2010). The gold standard test
for mycobacteria detection is 16S rDNA gene (Mijs et
al., 2002), but other targets have proven to be helpful, such as the internal transcribed spacer (ITS) region
and the hsp65 gene (Harmsen et al., 2003). The main
advantage of 16S rDNA gene analysis is that it can be
applied to all bacteria, including uncultivable or dead
bacteria (Harmsen et al., 2003).
For detection of MAC microorganisms, PCR searches for specific insertion sequences (IS900, IS901 and
IS1245) (Moravkova et al., 2008). Pavlik et al. (2000)
distinguished IS900 to M. a. paratuberculosis and IS901
or IS902 to M. a. silvaticum (Beggs et al., 2000). IS1141
to M. intracellulare and IS1110 to M. avium are also
described (Guerrero et al., 1995) (Table 2).
IS900 is a fragment repeated 15-20 times in all
strains of M. a. subsp. paratuberculosis’ genome
(Cousins et al., 1999; Coelho et al., 2007; Castellanos
et al., 2012). PCR assays for detection of IS900 are
highly sensitive to identify M. a. subsp. paratuberculosis (Kunze et al., 1992; Eriks et al., 1996; Whittington et al., 1998). However, to epidemiological studies,
strains differentiation is useful, which can be obtained
through Restriction Fragment Length Polymorphism
(RFLP) (Whittington et al., 1998). IS901 is specific
from M. avium serotypes 1, 2 and 3 isolates and there
are 2-13 copies in the genome (Dvorska et al., 2004).
The IS1245 was detected on isolates from bird sam-
ples, corresponding to M. avium subsp. avium (Mijs et
al., 2002), and are present 6-20 copies in isolates from
M. avium subsp. homnissuis (Dvorska et al., 2004).
Mycobacterium avium complex’ serotypes 7, 12-20
and 22-28 which don’t contain IS901 nor IS1245 were
designated M. intracellulare (Dvorska et al., 2004).
Restriction fragment length polymorphism
(RFLP) isn’t still currently used in epidemiological
studies about M. avium infections. There are 2 insertion sequences, IS1245 and IS1311, who shares
83-85% of DNA identity, consistently present in M.
avium and exhibit high RFLP diversity on human’s
isolates (Picardeau and Vincent, 1996; Whittington et
al., 1998).
Conclusion
The members of MAC are the most prevalent opportunistic pathogenic mycobacteria causing infection
both in animals and humans. Mycobacterium bovis is
the major responsible for tuberculosis in mammals.
The culture of mycobacteria is difficult and fastidious,
so other diagnosis strategies were developed. There
are specific PCR protocols which are reliable, fast and
cheap for the detection and differentiation of M. avium
subspecies and M. bovis, from solid plate cultures and
heavily infected tissues, for use in routine veterinary
diagnosis. It also contributes to increase the amount
of epidemiological studies, describing prevalence and
incidence of mycobacterial infections in wild populations and identification of maintenance hosts.
The study of mycobacteria in wild animals contributes to diminish the role of these animals as vectors on
the transmission to domestic animals and people.
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