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lajamjournal.org 211
ISSN: 2236-1057 | Vol. 19 No. 2, November 2024
ARTICLE INFO
Manuscript type: Article
Article History
Received: 30 March 2024
Received in revised form: 20 August 2024
Accepted: 20 August 2024
Available online: 24 November 2024
Handling Editor: Federic Riet Sapriza
Citation:
Antonelli, M., Ribas, M. R., Meurer, R., Sandri, S., Palmeiro, J. K.,
Sincero, T. C. M., & Kolesnikovas, C. K. M. (2024). Pseudomonas
aeruginosa sepsis in a neonate Franciscana dolphin (Pontoporia
blainvillei): clinical approach and laboratory findings. Latin American
Journal of Aquatic Mammals, 19(2), 211-218 . https://doi.org/10.5597/
lajam00338
Latin
American
Journal of
Aquatic
Mammals
Pseudomonas aeruginosa sepsis in a neonate
Franciscana dolphin (Pontoporia blainvillei): clinical
approach and laboratory ndings
Marzia Antonelli1,* , Mateus Rocha Ribas2, Rafael Meurer1, Sandro Sandri1,
Jussara Kasuko Palmeiro2, Thaís Cristine Marques Sincero2, and Cristiane
Kiyomi Miyaji Kolesnikovas1
1Associação R3 Animal, Florianópolis, Brazil
2Laboratório de Microbiologia Molecular Aplicada (MiMA), Universidade
Federal de Santa Catarina, Florianópolis, Brazil
*Corresponding author: marziaantonelli@gmail.com
Abstract
A neonate (4,2 kg and 71 cm total body length) female
Franciscana dolphin, Pontoporia blainvillei, was found stranded
alive on a beach in Santa Catarina, Southern Brazil, with
respiratory signs (dyspnea, crackles during thoracic auscultation
and changes in buoyancy) suggestive of pneumonia. Hand-
rearing and rehabilitation efforts were unsuccessful, and the
neonate died three days after it was rescued. Postmortem
investigation was conducted using diagnostic imaging
techniques, such as endoscopy and computed tomography. A
complete necropsy and histopathology were performed, revealing
bronchopneumonia as well as neutrophilic and discrete otitis
media. A pure Pseudomonas aeruginosa culture was obtained
from the blowhole, bronchoalveolar lavage, and blood using the
API NE System. Our results indicate the cause of death to be
related to bacterial sepsis. Further understanding of the main
causes of death of Franciscana dolphin calves is warranted
for conserving this threatened and understudied species.
Introduction
The Franciscana dolphin (Pontoporia blainvillei) is a small
cetacean endemic to the South Atlantic Ocean and restricted
to coastal waters, spanning from Brazil to Argentina. The
species is the only member of the family Pontoporiidae and
one of the most threatened cetaceans in South America, listed
as Vulnerable according to the International Union for the
Conservation of Nature – IUCN (Zerbini et al., 2018) due to its
well-acknowledged susceptibility to bycatch and as threatened
in the Brazilian Red List (Sucunza et al., 2023).
Rehabilitation of cetaceans poses signicant challenges due
to the aquatic environment, stress related to stranding, and
physiologic adaptations. Furthermore, deciencies in the immune
system make neonatal cetaceans susceptible to disease, and
mortality is a recognized concern in calves (Sweeney et al.,
2010; Flower et al., 2018).
Pseudomonas aeruginosa is an ubiquitous Gram-negative
bacterium commonly distributed across terrestrial and
aquatic environments globally, and it is prevalent in the natural
microbiota of numerous marine animals, including cetaceans.
Under conditions of immunosuppression, these bacteria may
transition to a pathogenic state, leading to the development
of consequential diseases, such as pneumonia and sepsis
(Buck et al., 2006; Pérez et al., 2015; Faure et al., 2018; Li et al.,
2019; Pelegrin et al., 2021; Reynolds & Kollef, 2021). Otitis is
often reported in domestic animals, caused by a wide variety
of pathogens, but is rarely documented in marine mammals
(Siebert et al., 2001; Wohlsein et al., 2019; Ready et al., 2021).
Clinicopathological evaluation in Franciscana dolphins is
complicated due to the non-existing normal range for blood
Keywords:
bacterial septicemia, cetacean, otitis, pneumonia, Pseudomonas
aeruginosa, rehabilitation, stranding event
lajamjournal.org 212
Vol. 19 No. 2, November 2024
values and imaging ndings. Additionally, there are only a
few reported cases of Franciscana’s clinical management
(Baldassin et al., 2007; Kolesnikovas, 2022; Meegan et al.,
2022). Here, we describe the rehabilitation efforts and clinical,
pathologic, microbiological, and diagnostic imaging ndings in
a Franciscana dolphin which stranded in Santa Catarina State,
Southern Brazil.
Materials and Methods
Case history and clinical ndings
A female Franciscana dolphin estimated to be a newborn,
around one week old (total body length: 71 cm, body weight: 4,2
kg, with umbilical cord, vibrissae on the rostrum and fetal lines),
stranded alive on the coast of Florianopolis, Santa Catarina
State, Brazil (27º39’05”S, 48º28’02”W) in November 2023. No
other animals were observed in the area, and the neonate was
transported to the R3 Animal Rehabilitation Facility for medical
care. Upon admission, the dolphin was extremely weak, and
signicant signs included dehydration, hypoglycemia, crackles
during thoracic auscultation, and dyspnea. The animal showed
changes in buoyancy and was unable to stay aoat unassisted.
The dolphin was placed in a seawater pool at 26 - 28ºC, with
a otation device to aid in buoyancy, and it was monitored 24
hours a day. Several diagnostic tests (hematological and blood
gas analysis, bacterial isolation, antimicrobial susceptibility
test from the blowhole swab) and diagnostic imaging (thoracic
ultrasound and radiography) were performed to establish the
most appropriate treatment. The initial respiratory rate was
ve breaths per minute, and the heart rate was 150 beats per
minute. Respiratory rate was measured every ve minutes,
and heart rate was measured when the animal was fed (every
hour). Preliminary blood analysis showed mild respiratory
alkalosis (pH: 7.635, and pCO2: 31.9 mmHg) and hemogram
values (Table 1) similar to a previous study (Baldassin et al.
2007). Blood glucose level was 50 mg/dl. Thorax radiographs
revealed a mild interstitial pattern and thoracic ultrasound
showed focal areas of a moderate alveolar interstitial syndrome.
During rehabilitation, antibiotics, uid therapy, and glucose were
administered, including intramuscular injection of ceftriaxone
(15 mg/kg s.i.d) and long-acting penicillin (50.000 IU every 72
hours). The neonate was tube-fed with 2 ml/kg of uids and milk
formula (Zoologic® Milk Matrix 30/52 PetAg Inc., Hampshire, IL,
USA, ltered water, dried egg whites and cetacean multivitamin)
hourly. On the third day in rehabilitation, the dolphin’s condition
had further deteriorated. It showed signs of abdominal and
respiratory discomfort, dyspnea, and began to vomit. Feeding
was temporarily halted and only uids were administered orally.
Intramuscular antiemetic, metoclopramide (0,1 mg/kg), oral
antispasmodic, and simethicone (2,0 mg/kg) were given twice.
Nebulization with aminophylline (2 mg/kg) and 0.9% NaCl (3
mL) driven by oxygen was conducted q.i.d. However, the animal
went into respiratory arrest and died on the same day.
Post-mortem diagnostic procedures
The dolphin carcass was refrigerated, and seven hours later an
endoscopy of the oral and nasal cavity and upper gastrointestinal
tract was performed using a rigid optic Hopkins® telescope
with a 30° vision angle, diameter of 2.7 mm, length of 18 cm
(Karl Storz SE & Co.), following standard protocols. After the
endoscopy, the dolphin was transported to a veterinary clinic
with a diagnostic imaging service, where a whole-body scan
(Figure 1a) was conducted using computed tomography (CT)
(Revolution CT from GE Healthcare).
Necropsy and histopathology
A complete necropsy was performed after the post-mortem
imaging procedures, the carcass was examined for external
lesions, and all organ systems were analyzed macroscopically.
Samples from most major organs and lesions were collected
and xed in 10% neutral buffered formalin for histological
examination. Tissue samples were embedded in paran-wax,
sectioned at 5 μm, and stained with hematoxylin and eosin for
Figure 1. Computed tomography (CT) ndings in a neonate female Franciscana dolphin Pontoporia blainvillei found stranded alive on a beach in
Santa Catarina, Southern Brazil. (a) The carcass was placed in a prone position for CT examination. (b)Transverse view from CT scan of the lungs
showing consolidation in the lower lungs (c) Transverse view from CT scan of the skull in P. blainvillei depicting occlusion of the left tympanic
bulla (red arrow).
lajamjournal.org 213
Vol. 19 No. 2, November 2024
Tab le 1. Hematological and blood gas values of neonatal female Franciscana dolphin (Pontoporiablainvillei), found stranded alive
on a beach in Santa Catarina, Southern Brazil.
RBC - red blood cell count; GV - globular volume; TTP - total plasma proteins; MCV - mean cell volume; MCH - mean corpuscular
hemoglobin; MCHC - cellular hemoglobin concentration mean; WBC - white blood cell count; PCO2 - carbon dioxide partial
pressure; PO2 - oxygen par tial pressure; TCO2 – total carbon dioxide; HCO3 – bicarbonate; BBecf - buffe r base ex tracell ular uid;
sO2 - oxygen saturation; iCa - ionized calcium; NA – not available.
Layer (Type)
Hematology and blood gas
RBC
Hemoglobin
GV
TTP
MCV
MCH
MCHC
WBC
Neutrophils
Neutrophils
Lymphocytes
Lymphocytes
Monocytes
Monocytes
Eosinophils
Eosinophils
Basophils
Basophils
Platelets
pH
PCO2
PO2
TCO2
HCO3
BEecf
sO2
Sodium
Potassium
iCa
Glucose
SI Units
1012 L-1
g L-1
(%)
g L-1
f L-1
pg
g L-1
109 L-1
%
109 L-1
%
109 L-1
%
109 L-1
%
109 L-1
%
109 L-1
109 L-1
mmHg
mmHg
mmol L-1
mmol L-1
mmol L-1
%
mmol L-1
mmol L-1
mmol L-1
mmol L-1
2023-11-05
4.03
158.8
46
72
114.14
39.40
345.2
4.50
61
2.74
36
1.62
0
0
3
135
0
0
60.60
7.635
31.9
82
35
34
1
98
156
4.3
1.12
3.33
2006-01-09
4.23
155
47
NA
111.1
36.64
329.7
4.20
60
2.52
35
1.47
2
0.084
2
0.084
0
0
189
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
2006-01-11
4.56
163
51
NA
111.84
35.74
319.6
3.50
60
2.10
30
1.05
5
0.175
3
0.105
0
0
155
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
This study Baldassin, P. et al., 2007
2006-01-13
4.77
177
55
NA
115.30
37.10
321.8
0.90
68
0.612
28
0.252
3
0.027
0
0
0
0
120
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
lajamjournal.org 214
Vol. 19 No. 2, November 2024
microscopic analysis.
Microbiology and molecular diagnosis
During the necropsy, the blowhole, blood, and bronchoalveolar
lavage samples were aseptically collected and submitted for
bacteriological culture. Blowhole and bronchoalveolar lavage
samples were inoculated onto Columbia agar (Kasvi) with
5% sheep blood and MacConkey agar (Kasvi) and incubated
overnight at 35±2°C. Blood samples were aseptically collected
from the heart and stored in blood culture bottles (NewProv)
broth at 35±2°C for 24 h before subculturing onto the culture as
mentioned above. After isolation, the bacterial strain underwent
identication using the API NE System (bioMérieux). After
identifying the bacterial isolate, antimicrobial susceptibility
testing was conducted using the disk diffusion method (Bauer et
al., 1966). Discs (Oxoid and Liolchen) containing Cephalosporins
(Cefepime 30 μg, Ceftazidime 30 μg), Carbapenems (Imipenem
10 μg, Meropenem 10 μg), Monobactam (Aztreonam 30 μg),
Quinolone (Ciprooxacin 5 μg), and Aminoglycoside (Amikacin
30 μg) were utilized for the tests. The zone diameter breakpoints
were evaluated in accordance with the CLSI (2023) guidelines.
Tympanic bulla swabs were not collected due to contamination of
the site after opening the skull during the necropsy examination.
Reverse Transcription Polymerase chain reaction (RT-PCR)
testing for Morbillivirus sp. and PCR testing for Brucella spp.
were performed on frozen samples (adrenal gland, brain, heart,
liver, lungs, lymph nodes, and spleen) as previously described
(Tong et al., 2008; Batinga et al., 2018).
Results
The endoscopic evaluation of the cranial esophagus revealed
the presence of milk formula and mild esophageal hyperemia,
suggesting gastro-esophageal reux, and the presence of
anterolateral mechanical papillae were observed on the tongue
apex. Slight streaks of blood were found through blowhole
endoscopy. The CT scan revealed pneumonia in the cranioventral
lung regions (Figure 1b), uid material in the esophagus, and
soft tissue opacity in the left tympanic bulla (Figure 1c).
At the necropsy, the subcutaneous tissue was pale yellow
and congested. The intrathoracic pressure was decreased, and
the main lesions were observed in the lungs. The tissue of the
caudal dorsal quadrant collapsed, and multifocal, white, small
punctate nodules were observed in the parenchyma, along
with congestion of both lungs (Figure 2a). The esophageal
mucosa was hyperemic, and pasty content was found within
the lumen. The liver was enlarged. The intestines, kidneys, and
stomach were congested. The left tympanic-periotic complex
was extracted from the paraotic sinus, revealing congestion
and yellow purulent material in tympanic bullae (Figure 2b, c).
No internal or external parasites were recorded.
Microscopically, there was moderate congestion of the
mucosa and serosa of the large intestine, and in the gastric
mucosa and submucosa. Additionally, splenic, renal, thymic,
and brain parenchyma were congested. A discrete inltration
of neutrophils permeated by discrete eosinophilic brillar
material (brin) was observed in the left tympanic bulla. The
lungs showed moderately expanded alveoli, with discrete to
moderate neutrophil inltration and macrophages permeated
with fragments of laminar keratin.
All bacterial cultures revealed pure growth of Pseudomonas
aeruginosa, and the result of the antimicrobial susceptibility
testing showed no resistance to any of the tested antimicrobials.
PCR tests were all negative for Morbillivirus sp. and Brucella
spp.
Discussion
The Franciscana dolphin is a threatened cetacean whose
main cause of strandings and death is bycatch. Most cases of
live-stranded Franciscana dolphins are neonates, which survive
Figure 2. Gross lesions of a neonate female Franciscana dolphin, Pontoporia blainvillei, found stranded alive on a beach in Santa Catarina, Southern
Brazil diagnosed with pneumonia and otitis (a) lungs, ventral view, showing congestion (b). Left tympanic bulla with suppurative material (black
head arrows), view upon the ventral aspect of the skull. (c) Left tympanic bulla removed from the skull, showing suppurative material content
(black arrow).
lajamjournal.org 215
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only a few hours or days. Providing food for neonatal cetaceans
that meets nutritional requirements and has good digestibility
is a challenge. We tested a formula based on published work
(Baldassin et al., 2007; Flower et al., 2018), but the results found
suggest the need for new adaptations of the current formula
recipe and future studies on nutritional protocols for P. blainvillei
calves. To date, only two juvenile Franciscana dolphins have been
successfully released in Brazil, and every effort to rehabilitate a
live animal provides valuable information for future strandings
(Kolesnikovas, 2022; Meegan et al., 2022).
In marine mammals, bacterial respiratory system infections
signicantly contribute to morbidity and mortality. Pneumonia
is one of the most common pathologies reported in dolphins,
and several pathogens have been associated with respiratory
diseases in cetaceans (Bogomolni et al., 2010; Venn-Watson
et al., 2012; Venn-Watson, 2016; Elfadl et al. 2017). Aspiration
pneumonia, gastroesophageal reux, infections, and sepsis
are among the principal problems in neonates (Sweeney et
al., 2010; Pérez et al., 2015; Díaz-Delgado et al., 2018; Flower
et al., 2018). Herein, an endoscopic examination of the oral
cavity demonstrated the presence of anterolateral mechanical
papillae arranged on the tongue apex, described in neonatal
and juvenile individuals of P. blainvillei (Tostado-Marcos et
al., 2024). Following what we observed in the reported case,
thoracic ultrasound is a valuable diagnostic method for detecting
pulmonary diseases (Smith et al., 2012), and endoscopy and
CT can be used for post-mortem investigation (Venn-Watson
et al., 2012; Tsui et al., 2020; García de los Ríos y Loshuertos
et al., 2021; Ready et al., 2021).
Diagnosing diseases in marine mammals is often challenging,
even when clinical signs are present (Souter et al., 2024). Timely
and appropriate therapy frequently fails to yield successful
outcomes. The coexistence of bacteria with viruses and parasitic
infections complicates determining their role as primary or
secondary pathogens (Simeone & Stoskopf, 2018; Haebler
& Moeller, 2021). In cases of bacterial respiratory disease,
antibiotic selection should follow routine culture and sensitivity
characterization, often starting before test results are available.
Broad-spectrum antibiotics effective against Gram-negative
organisms are commonly used initially (Simeone & Stoskopf,
2018).
However, the rapid progression of infections, coupled with
clinical deterioration exacerbated by factors like stress, adds
complexity to clinical management. Unfortunately, bacterial
culture and susceptibility testing results are often known only
after an animal’s death.
The initial treatment selected for the reported animal included
the administration of ceftriaxone, followed by penicillin. These
antimicrobials can effectively target beta-lactam-susceptible
Enterobacterales and penicillin-susceptible Gram-positive bacteria
(Cheng et al., 2016). This enables the treatment of primary
and secondary infections associated with a diverse range of
pneumonia-associated agents (da Trindade & Salgado, 2018).
Additionally, ceftriaxone can be utilized in combating erysipelas,
caused by Erysipelothrix rhusiopathiae, which is considered one
of the most severe bacterial infections in cetaceans worldwide
(Fidalgo et al., 2002; Tryland et al., 2018; Lee et al., 2022).
Despite efforts to use antimicrobials, post-mortem results
indicated that the cetacean exhibited a widespread infection
caused by Pseudomonas aeruginosa. This agent is a known
opportunistic bacterium found in marine mammal infections
(Venn-Watson et al., 2012) and was one of the most common
species isolated in humans and domestic animals diagnosed
with otitis (Shyamala R & Reddy, 2012; de Melo, 2019).
Furthermore, this bacterium presents a broad range of intrinsic
antimicrobial resistance in its chromosome, and the use of
Penicillin and Ceftriaxone was not effective in combating this
infection (Karruli et al., 2010).
Unfortunately, it was not possible to identify the bacterial
species before the rapid clinical progression of the infection.
In this scenario, using ceftazidime or cefepime as substitutes
for ceftriaxone could have been more effective in treating
the infection and, at the same time, impacting beta-lactam-
susceptible Enterobacterales. Both medications are applicable
in the treatment of infections in cetaceans, indicating that an
adaptation to the internal protocol could represent a viable
alternative to encompass a wider variety of pneumonia-
causing agents in these animals (Simeone & Stoskopf, 2018).
Furthermore, maintaining the use of Penicillin can aid in
combating potential infections of E. rhusiopathiae (Reboli &
Farrar, 2010).
Otitis media is an accumulation of exudate and debris in
tympanic bulla and represents a disease often reported in
domestic animals caused by a wide variety of etiologies. In
contrast, it is rarely documented in marine mammals, with
most cases being post-mortem ndings on stranded cetaceans
and incidentally ndings in live stranded pinnipeds (Siebert et
al., 2001; Ready et al., 2021). In Phocoena phocoena, otitis was
reported to be associated with parasite infestation, chronic
inammation, hyperplastic, and metaplastic epithelial changes
(Wohlsein et al., 2019). Penicillium spp. was identied by
molecular analysis in a Tursiops truncatus with pyogranulomatous
and necrotizing otitis media, and mycotic otitis has also been
seen in P. phocoena (Seibel et al., 2010; Attig et al., 2018; Van Elk
et al., 2019). In our reported case, no parasites or fungal hyphae
were found in the tympanic cavity and ear structures. Otitis was
initially identied by CT, a useful technique to diagnose middle
ear diseases in domestic and marine mammals (Parlak et al.,
2021; Ready et al., 2021).
Diagnostic imaging ndings, clinicopathological evaluations,
and microbiological assessments allowed the diagnosis of P.
aeruginosa pneumonia and sepsis in the Franciscana dolphin.
Additionally, the neonate exhibited mild to moderate neutrophilic
and histiocytic bronchopneumonia associated with fragments
of laminar keratin, though this can be an incidental nding in
calves (Van Elk et al., 2007). Neonate’s immature immune system
may have contributed to otitis media and septicemia. There is
a scarcity of information about Pontoporia blainvillei’s natural
parameters and pathogens, and further research is needed to
advance our understanding of their natural causes of disease
and mortality. Furthermore, trying to rehabilitate individuals
of such endangered populations would contribute to future
conservation efforts.
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Vol. 19 No. 2, November 2024
Acknowledgments
The authors thank the anonymous reviewers and editors of
LAJAM journal for their helpful comments to the manuscript; Ana
Carolina Santos Ibanez, Jenny Meegan, and Ricardo Fernandes
Bernardo for their assistance with diagnostic imaging; Daniela
Farias da Nóbrega (Pat Animal Lab) for histopathology services
and Lara Borges Keid (ZMV-FZEA-USP) for molecular diagnosis.
This research was supported by The Alliance for Franciscana
Research and Protection and The Santos Basin Beach Monitoring
Project (Projeto de Monitoramento de Praias da Bacia de Santos
— PMP-BS), conducted from Laguna/SC to Saquarema/RJ, a
requirement set by the Brazilian Institute of the Environment
(IBAMA) for the environmental licensing of the oil and natural
gas production and transport by Petrobras. All biological data
were collected under the IBAMA license (ABIO n°640/2015).
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