Wischnewski Spots in Monkey and Rabbit

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J. Comp. Path. 2021, Vol. 186, 18e22 Available online at www.sciencedirect.com
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FORENSIC MATTERS
Wischnewski Spots and Black Oesophagus in
Suspected Fatal Hypothermia in a Brown Howler
Monkey (Alouatta guariba clamitans) and a Rabbit
(Oryctolagus cuniculus)
Cor
002
http
Bruno A Almeida*, Igor R Santos*, Luan C Henker*,
Marina P Lorenzett*, Fl�avia E Ferrari†, Lı́via E Surita†,
Welden Panziera*, Saulo P Pavarini* and David Driemeier*
*Setor de Patologia Veterin�aria and †N�ucleo de Conservaç~ao e Reabilitaç~ao de Animais Silvestres, Universidade Federal do Rio
Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
resp
1-99
s://
Summary
Fatal hypothermia represents a diagnostic challenge in veterinary pathology. Wischnewski spots (WS) and
black oesophagus (BO) have been described in human cases of fatal hypothermia but rarely in animals. We
now describe WS and BO in suspected fatal hypothermia in a free-ranging brown howler monkey (Alouatta
guariba clamitans) and a pet rabbit (Oryctolagus cuniculus). Both animals had dark spots resembling WS on the
gastric mucosa and the monkey also had BO with haematin deposition. In both cases, stress factors and rela-
tively cold environmental conditions were present prior to death.
� 2021 Elsevier Ltd. All rights reserved.
Keywords: acute oesophageal necrosis; black spots; forensic pathology; gastric mucosa
Hypothermia is an uncommon and challenging diag-
nosis in veterinary medicine (Wohlsein et al, 2016). In
humans, Wischnewski spots (WS) on the gastric mu-
cosa and reddishebrown erythematous discoloura-
tion of the skin of the extensor surface of the larger
joints are generally considered to be indicative of hy-
pothermia (Palmiere et al, 2014). WS have been re-
ported in 43.5e100% of humans with fatal
hypothermia (Gwaltney-Brant, 2016; Wohlsein et al,
2016). Although rarely described in animals, this
lesion has been documented in two dogs found dead
in an extremely cold environment (Stern and
Vieson, 2017). WS are due to body cooling in low
environmental temperatures and are characterized
by discrete, circumscribed haemorrhages on the
gastric mucosa. Due to autolysis and erythrocyte lysis,
ondence to: B A Almeida (e-mail: brunoadealmeida@live.com).
75/$ - see front matter
doi.org/10.1016/j.jcpa.2021.05.001
released haemoglobin exposed to gastric acid becomes
haematinized (Palmiere et al, 2014). Histologically,
WS are distinguished from mucosal erosions and ul-
cerations by the absence of inflammatory infiltrates,
fibrin exudates or other vascular changes (Tsokos
et al, 2006), and are classified as a periagonal,
hypothermia-related phenomenon (Ball and
Herath, 2018). Acute oesophageal necrosis, also
known as black oesophagus (BO), is associated with
upper gastrointestinal bleeding (Gurvits et al, 2007)
but is rarely associated with fatal hypothermia in hu-
mans and has not been described in animals.
Due to limited information and the importance of
this finding for surveys of wildlife mortality, forensic
veterinary and veterinary pathology, the aim of this
report is to describe WS and BO in a free-ranging,
adult male brown howlermonkey (Alouatta guariba cla-
mitans) and WS in a 5-year-old male pet rabbit
� 2021 Elsevier Ltd. All rights reserved.
https://doi.org/10.1016/j.jcpa.2021.05.001
https://doi.org/10.1016/j.jcpa.2021.05.001
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mailto:brunoadealmeida@live.com
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Fig. 2. Brown howler monkey, oesophagus, suspected fatal hypo-
thermia. Black oesophagus characterized by dark linear
discolourations merging into the cardia (top). Bar, 1 cm.
Wischnewski Spots and Black Oesophagus in Suspected Fatal Hypothermia 19
(Oryctolagus cuniculus), both of which had suspected
fatal hypothermia.
Systematic necropsies were performed on both an-
imals and samples of various tissue organs fixed in
10% neutral buffered formalin, processed routinely
and stained with haematoxylin and eosin (HE). The
time that had elapsed between death and post-
mortem examination was estimated according to the
degrees of rigor mortis and decomposition, and from
entomological evidence (Brooks, 2016).
The brown howler monkey had been rescued in
Rio Grande do Sul during the winter of 2020 but
had died after arrival at a veterinary clinic where
the carcass was frozen (�20�C). Environmental tem-
peratures at the time of death could not be retrieved
for this case, but the monkey died after the first two
waves of cold, in which morning temperatures had
reached 9�C (thermal sensation 7.7�C). The winter
dawn temperature in the capital of Rio Grande do
Sul ranged from 2.6�C to 26.7�C in 2020.
Grossly, the monkey had poor body condition with
minimal fat reserves, prominent hip bones and
spinous processes and the main lesions were located
in the oesophageal and gastric mucosae. The esti-
mated post-mortem interval was 6e36 h due to the
presence of full rigor mortis and the absence of carcass
discolouration due to autolysis, blowfly eggs or insect
activity on the carcass. The gastric mucosa hadmulti-
focal dark spots (0.1e1.0 cm in diameter) (Fig. 1),
while dark longitudinal linear, often coalescing, le-
sions were present on the oesophageal mucosa
(Fig. 2). Histologically, there were multifocal amor-
phous to U- and V-shaped areas of rarefaction of
epithelial cells with marked golden browneblack
extracellular haematin deposition without any in-
Fig. 1. Brown howler monkey, stomach, suspected fatal hypother-
mia. Random dark brown Wischnewski spots on mucosa.
Bar, 5 cm.
flammatory reaction or fibrin deposition (Fig. 3).
Despite a similar gross appearance, the oesophagus
had ulceration, characterized by loss of mucosa with
multifocal fibrin deposition and a suppurative inflam-
matory reaction, associated with submucosal haema-
tin deposition (Supplementary Fig. 1). The monkey
also had several microfilariae in the thoracic and
abdominal cavities and a heavy Trypanoxyuris spp
infestation in the caecum. Based on the pathological
findings, circumstantial evidence of exposure to low
environmental temperatures and lack of other lethal
factors, a diagnosis of fatal hypothermia was made.
The rabbit had a history of recent trauma and clin-
ical examination revealed that it had multiple frac-
tures and was anorexic, prostrate, hypothermic
Fig. 3. Brown howler monkey, stomach, suspected fatal hypother-
mia. Wischnewski spot in gastric mucosa, characterized by
V-shaped area with moderate haematin deposition. HE.
Bar, 200 mm.
20 B A Almeida et al
(36�C; reference interval [RI], 38.5e40�C [Varga,
2014]) and dehydrated, as indicated by a marked in-
crease in skin turgor and dry oral mucousmembranes.
Laboratory assessment revealed anaemia (haematoc-
rit, 25%; RI, 30e40% [Melillo, 2007]) and hypopro-
teinaemia (total protein, 50 g/l; RI, 54e75 g/l
[Melillo, 2007]). Despite efforts to warm up the ani-
mal and other supportive measures, the animal died
the following night and was referred for necropsy,
before which the carcass had been maintained at
7�C. The minimum outside temperatures on the
days of the traumatic injury and death were 9.1�C
and 4.2�C, respectively (Instituto Nacional de Mete-
orologia, automatic station A801, Porto Alegre,
Brazil). At post-mortem examination, haemorrhages
were seen to be associated with multiple comminuted
fractures of the femurs, tibias, fibulas, left mandibular
ramus and top of cranium. The time between death
and necropsy was estimated at approximately 36 h,
based on the degree of the rigor mortis in the muscles
of the jaw and upper extremities and absence of rigor
in the lower extremities, carcass discolouration,
blowfly eggs or insect activity.
Round to oval, random dark browneblack spots
(0.1e0.4 cm diameter) were seen on the gastric mu-
cosa (Fig. 4). Histologically,principal cells were
rare and parietal cells were absent within the lesioned
area. Individualized parietal cells were frequently py-
knotic and karyolytic. At the periphery, principal
cells had pyknotic nuclei and sloughing cytoplasm,
whereas nuclear degeneration of parietal cells was
rare. The lesions were frequently U- or V-shaped,
or amorphous, and haemorrhage and moderate hae-
matin deposition were also seen (Supplementary
Fig. 2) without evidence of inflammation. The right
adrenal gland was enlarged (2.5 cm diameter) and
irregular with the parenchyma replaced by a homo-
Fig. 4. Rabbit, stomach, suspected fatal hypothermia. Random
dark brown Wischnewski spots on mucosa. Bar, 7 cm.
geneous yellow mass. Microscopically, this mass was
identified as a circumscribed adrenocortical carci-
noma. A diagnosis of fatal hypothermia, secondary
to cold exposure and trauma, was determined on
the basis of environmental temperature and clinical
and pathological findings.
WS result from a combination of environmental
and physiological factors and have been rarely docu-
mented in animals. To the authors’ knowledge, this is
only the second description of WS in animals and the
first report of BO associated with suspected fatal hy-
pothermia in animals.
WS are commonly found in humans after stressful
events associated with fatal hypothermia (Bright
et al, 2013). Predisposing factors, including damp con-
ditions, muscle mass loss, trauma, age, alcohol con-
sumption and drug use, are associated with an
increased risk of hypothermia in humans. Starvation
and lymphoma have been associated with fatal hypo-
thermia and WS-like lesions in dogs (Stern and
Vieson, 2017). The brown howler monkey is widely
distributed in Brazil’s coastal states within the
Atlantic forest domain (Culot et al, 2019). Low winter
temperatures are believed to define the southern
geographic limit for South American primates
(Printes et al, 2019). The monkey of this report was
found near the geographic limit during wintertime
in Rio Grande do Sul, which is the southernmost state
of Brazil, and which has well-defined seasons
(Conrado et al, 2014). No comorbidities, other than
severe parasitism, were detected in this monkey. Pri-
mates seem to be relatively vulnerable to parasite
infestation due to their social behaviour, which pre-
disposes them to parasite transmission (Stoner,
1996). Heavy Trypanoxyuris minutus infestation has
been associated with the death of a brown howler
monkey (Amato et al, 2002). However, in our report,
the heavy parasitism was probably a stress factor, as
blood loss is a recognized factor that can predispose
to fatal hypothermia (Thorsen et al, 2011).
The rabbit had an adrenal tumour and was
severely traumatized. The extensive traumatic in-
juries in the rabbit could have resulted in immobiliza-
tion and hypothermia due to the inability to reach
shelter (Zafren, 2012). The thermal comfort zone of
healthy rabbits is w21�C (Marai et al, 2002),
although a minimum temperature of w10�C for out-
door healthy rabbits with accessible shelters has been
reported for non-freezing cold environments (Lebas
et al, 1986). The reported environmental temperature
at the time of death of this rabbit was only slightly
below the recommended level, but does not take ac-
count of thermal sensation, in whichwind and humid-
ity can lower body temperature. Establishing a
predisposing stress factor in free-ranging and pet
Wischnewski Spots and Black Oesophagus in Suspected Fatal Hypothermia 21
animals can be difficult but is useful for making a
diagnosis of fatal hypothermia.
The macroscopic lesions observed in the stomach
and oesophagus had similar characteristics, although
with different distribution patterns. Multifocal WS
and coalescent dark lines in the oesophagus have
been described in fatal hypothermia in humans
(�Zivkovi�c and Nikoli�c, 2013). The gastric mucosal le-
sions have also been described as a ‘leopard skin’
pattern (Bright et al, 2013). Histologically, the grossly
visibly dark lines in the oesophagus represent sharp-
edged mucosal necrosis with microscopically evident
neutrophilic infiltrate (�Zivkovi�c and Nikoli�c, 2013),
often extending to the submucosa (Brennan, 1967).
The susceptibility of the oesophageal stratified squa-
mous epithelium to damage from gastric secretions
could explain the livid lesions in the oesophagus, as
it has been demonstrated that a relatively short expo-
sure of oesophageal epithelium to corrosive gastric
secretion induces hyperaemia, linear erosions or ul-
cers with superficial fibrinonecrotic debris (Uzal
et al, 2016). In contrast, the gastric mucosa is much
more resistant to gastric secretions. BO is associated
with a combination of hypoperfusion, reduced local
defences and reflux of gastric contents (Gurvits et al,
2007). Hypoperfusion is a common consequence of
low blood flow following acute haemorrhage or hypo-
thermia (Brennan, 1967; Gurvits et al, 2007).
Our histological findings correspond to previous
descriptions of WS as V- or U-shaped or amorphous
areas in the gastric mucosa (Dettmeyer, 2018), which
can be haematinized after the interaction of haemo-
globin and gastric secretion (Tsokos et al, 2006).
Furthermore, the lack of erosions, inflammatory reac-
tion, ulceration or other ante-mortem injury or
response support the view that WS are a periagonal,
hypothermia-related tissue change (Tsokos et al,
2006). Immunohistochemical investigation has re-
vealed diffuse labelling of haemoglobin in WS
(Tsokos et al, 2006). Although we did not perform
immunohistochemistry to confirm the origin of the
pigment, the presence of erythrocytes in association
with the other findings suggest it was haematin.
Carcass freezing prior to post-mortem examination
is considered unlikely to cause this change (Stoner,
1996), and corpse cooling or freezing has not been
associated withWS or BO formation in humans or an-
imals. As in the report on dogs (Stoner, 1996), stress
factors and harsh environmental conditions were
likely associated with the gastric and oesophageal
changes in this rabbit and monkey.
Acknowledgments
This study was supported by the Conselho Nacional
de Pesquisa and Coordenaç~ao de Aperfeiçoamento
de Pessoal de Nı́vel Superior.
Conflict of Interest Statement
The authors declared no conflicts of interest with
respect to the research, authorship or publication of
this manuscript.
Supplementary data
Supplementary data to this article can be found on-
line at https://doi.org/10.1016/j.jcpa.2021.05.001.
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Update
Journal of Comparative Pathology
Volume 187, Issue , August 2021, Page 1
 https://doi.org/10.1016/j.jcpa.2021.06.001DOI:
 https://doi.org/10.1016/j.jcpa.2021.06.001
J. Comp. Path. 2021, Vol. 187, 1e1 Available online at www.sciencedirect.com
ScienceDirect
www.elsevier.com/locate/jcpa
CORRIGENDUM
Corrigendum to “Wischnewski Spots and Black
Oesophagus in Suspected Fatal Hypothermia in a
Brown Howler Monkey (Alouatta guariba
clamitans) and a Rabbit (Oryctolagus cuniculus)”
[Journal of Comparative Pathology (186) (July 2021)
Pages 18e22]
DO
Cor
002
http
Bruno A Almeida*, Igor R Santos*, Luan C Henker*,
Marina P Lorenzett*, Fl�avia E Ferrari†, Lı́via E Surita†,
Welden Panziera*, Saulo P Pavarini* and David Driemeier*
*Setor de Patologia Veterin�aria and †N�ucleo de Conservaç~ao e Reabilitaç~ao de Animais Silvestres, Universidade Federal do Rio
Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
The authors regret the following errors in citation of references in this article and would like to apologise for any
inconvenience caused:
Page 18, left column: ‘(Gwaltney-Brant, 2016; Wohlsein et al, 2016)’ should read ‘(Bright et al, 2014; Mizu-
kami et al, 1999)’.
Page 18, right column: ‘(Palmiere et al, 2014)’ should read ‘(Tsokos et al, 2006; Palmiere et al, 2014)’.
Page 21, left column, last paragraph: Each mention of ‘(Stoner, 1996)’ should read ‘(Stern and Vieson,
2017)’.
The bibliography to this article should include the following additional references:
Bright FM, Winskog C, Tsokos M, Walker M, Byard RW (2014) Issues in the diagnosis of hypothermia: a
comparison of two geographically separate populations. Journal of Forensic and Legal Medicine, 22, 30e32.
Mizukami H, Shimizu K, Shiono H, Uezono T, Sasaki M (1999) Forensic diagnosis of death from cold. Legal
Medicine, 1, 204e209.
Uncited Reference
Gwaltney-Brant SM (2016) Veterinary forensic toxicology. Veterinary Pathology, 53, 1067e1077.
I of original art
respondence to
1-9975/$ - see f
s://doi.org/10.1
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eceived, June 7th, 2021
ccepted, June 14th, 2021
e: https://doi.org/10.1016/j.jc
A Almeida (e-mail: brunoad
t matter
6/j.jcpa.2021.06.001
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pa.2021.05.001.
ealmeida@live.com).
� 2021 Elsevier Ltd. All rights reserved.
https://doi.org/10.1016/j.jcpa.2021.06.001
https://doi.org/10.1016/j.jcpa.2021.06.001
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https://doi.org/10.1016/j.jcpa.2021.05.001
mailto:brunoadealmeida@live.com
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	Wischnewski Spots and Black Oesophagus in Suspected Fatal Hypothermia in a Brown Howler Monkey (Alouatta guariba clamitans) ...
	Acknowledgments
	Conflict of Interest Statement
	Appendix A. Supplementary data
	References
	Update
	Corrigendum to “Wischnewski Spots and Black Oesophagus in Suspected Fatal Hypothermia in a Brown Howler Monkey (Alouatta gu ...