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Anatomy of the paranasal sinuses of the common marmoset (Callithrix jacchus Linnaeus, 1758) and radiographic positioning for diagnosis of these structures

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Common marmosets (Callithrix jacchus) are anthropoid primates belonging to the Cebidae family and subfamily Callitrichinae. 1 They are small animals, with weight ranging from 300 to 450 g and that adapt well to life in captivity.2 They are endemic animals from Brazil, being found in the Amazon forest, southeast and northeast of Brazil.3 Trafficking wild animals currently represents one of the main threats to the lives of countless animals that make up the Brazilian fauna, including in this situation the common marmosets, which, due to their good adaptation to captivity and small size, have become one of the choices of those who want to raise animals other than domestic ones. The conditions that the animals are put through by the traffic greatly deteriorate their health, as they are kept in tight places, without ventilation and without access to water or food until they reach their final destination. During this process, many of the animals die and others, when Received: 26 May 2020  |  Revised: 17 August 2020  |  Accepted: 3 September 2020 DOI: 10.1111/jmp.12496 ORIGINAL ARTICLE Anatomy of the paranasal sinuses of the common marmoset (Callithrix jacchus Linnaeus, 1758) and radiographic positioning for diagnosis of these structures Joyce Galvão de Souza1 | Moana Barbosa dos Santos Figuerêdo2 | Brunna Muniz Rodrigues Falcão1 | Luan Nascimento Batista2 | Artur da Nóbrega Carreiro1 | Débora Vitória Fernandes de Araújo2 | Temístocles Soares de Oliveira Neto2 | Gildenor Xavier Medeiros1,2 © 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Institution in which work was performed: Laboratory of Morphological Research, Federal University of Campina Grande – Patos, PB, Brazil 1Postgraduate Program in Animal Science and Health, Federal University of Campina Grande, Patos, Brazil 2Veterinary Medicine Academic Unit, Federal University of Campina Grande, Patos, Brazil Correspondence Joyce Galvão de Souza, Federal University of Campina Grande; , Patos, PB, Brazil. Email: Abstract Background: Callithrix jacchus, it is a species highly targeted by wild animal traffickers and, when apprehended, they need veterinary care. For safe therapeutic procedures, knowledge of anatomy is essential, as well as for diagnostic by imaging, good radiographic positioning is essential. Methods: The anatomy of the paranasal sinuses and the radiographic projections was described using 10 carcasses of common marmosets. Radiographs were taken in two panoramic views of their head: profile and frontal-naso. For the anatomical study, paramedian and transverse macroscopic sections and microscopic transverse sections were performed. Results: On the radiographs, it was possible to identify the frontal recess and maxillary sinuses in profile and frontal-naso incidences. In the anatomical study, the frontal recess and maxillary, sphenoid and ethmoid paranasal sinuses were identified. Conclusions: The ethmoidal sinus could be observed only microscopically and the sphenoidal sinus difficult to see on the radiography due to the overlapping adjoining structures. KEYWORDS Callitrichinae, primates, respiratory system 2  |    de SOUZA et Al. apprehended by agents from the Brazilian Institute for the Environment and Renewable Natural Resources (IBAMA) and sent to the Wild Animal Screening Centers (CETAS), require veterinary medical care.4 One of the main systems of the animal organism frequently affected in primates is the respiratory system, which is extremely important for the maintenance of life,5 and several pathologies can affect this system, such as, infectious inflammatory diseases or not, neoplasms, dental diseases, trauma, parasitic diseases, all of which can cause changes in the respiratory system.6 The knowledge of the paranasal sinuses and the nasal cavity, in addition to their variations, is of great importance for the diagnosis of pathologies such as rhinosinusitis for example, and for surgical access of these structures in human medicine,7 and may be applied to veterinary medicine. Knowledge about the relationship between the paranasal sinuses and the skull and its morphological variations are of great importance for understanding the function of this structure,8 as there are still disagreements among several authors about the real function that the paranasal sinuses develop in the animal organism, as well as there is still uncertain point about the development of pneumatization in the facial skeleton.9 And, when compared to Old World primates, there are a lower number of studies that seek to bring information about the paranasal sinuses of New World primates.10 The studies carried out with paranasal sinuses of platyrrhini primates have the potential to help in the search for knowledge about the function of the sinuses due to the great morphological variation found in the several species of this group, acting as a natural experiment.11 Imaging examinations of the paranasal sinuses can help in the identification and knowledge of the extent of morphological variations, bone changes, or the presence of ectopic soft tissues.12 The radiographic diagnostic method is widely used within veterinary medicine because it has several advantages, such as the benefit-cost ratio, being one of the most important diagnostic methods for identifying various conditions that affect animals, however, so that the greatest benefit from this tool is achieved, it is necessary the best application of specific techniques in order to obtain a superior quality image.13 Despite the increase in the use of more advanced techniques such as computed tomography in several institutions, in Brazil, it has not yet become a widely accessible technique for use in wild animals, either due to the higher cost or the unavailability of equipment in several regions, making it necessary to resort to often to the use of conventional or computerized radiographs, which can be used as screening tests and which will facilitate in a better direction of diagnosis or for the performance of other complementary tests, when available. Therefore, our objective with this study was to identify the anatomy of the paranasal sinuses and define the incidence plans for radiographic examinations in common marmosets. 2 | MATERIAL AND METHODS Ten carcasses of common marmosets (C jacchus)—adults, composed of five females and five males donated by the CETAS/ IBAMA in the city of Cabedelo, Paraíba, Brazil—were used at the Veterinary Anatomy Laboratory, from the Health Center and Rural Technology, Federal University of Campina Grande (LAV/ CSTR/UFCG). The project was

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Received: 26 May 2020 | Revised: 17 August 2020 | Accepted: 3 September 2020

DOI: 10.1111/jmp.12496


ORIGINAL ARTICLE




Anatomy of the paranasal sinuses of the common marmoset
(Callithrix jacchus Linnaeus, 1758) and radiographic positioning
for diagnosis of these structures

Joyce Galvão de Souza1 | Moana Barbosa dos Santos Figuerêdo2 |
1
Brunna Muniz Rodrigues Falcão | Luan Nascimento Batista2
|
1
Artur da Nóbrega Carreiro | Débora Vitória Fernandes de Araújo2 |
1,2
Temístocles Soares de Oliveira Neto2
| Gildenor Xavier Medeiros

1
Postgraduate Program in Animal Science
and Health, Federal University of Campina Abstract
Grande, Patos, Brazil Background: Callithrix jacchus, it is a species highly targeted by wild animal traffickers
2
Veterinary Medicine Academic Unit,
and, when apprehended, they need veterinary care. For safe therapeutic procedures,
Federal University of Campina Grande,
Patos, Brazil knowledge of anatomy is essential, as well as for diagnostic by imaging, good radio-
graphic positioning is essential.
Correspondence
Joyce Galvão de Souza, Federal University Methods: The anatomy of the paranasal sinuses and the radiographic projections
of Campina Grande; 58708-110, Patos, PB,
was described using 10 carcasses of common marmosets. Radiographs were taken
Brazil.
Email: in two panoramic views of their head: profile and frontal-naso. For the anatomical
study, paramedian and transverse macroscopic sections and microscopic transverse
sections were performed.
Results: On the radiographs, it was possible to identify the frontal recess and maxil-
lary sinuses in profile and frontal-naso incidences. In the anatomical study, the frontal
recess and maxillary, sphenoid and ethmoid paranasal sinuses were identified.
Conclusions: The ethmoidal sinus could be observed only microscopically and the
sphenoidal sinus difficult to see on the radiography due to the overlapping adjoining
structures.

KEYWORDS

Callitrichinae, primates, respiratory system



1 | I NTRO D U C TI O N Trafficking wild animals currently represents one of the main threats
to the lives of countless animals that make up the Brazilian fauna, in-
Common marmosets (Callithrix jacchus) are anthropoid primates cluding in this situation the common marmosets, which, due to their
1
belonging to the Cebidae family and subfamily Callitrichinae. They good adaptation to captivity and small size, have become one of the
are small animals, with weight ranging from 300 to 450 g and that choices of those who want to raise animals other than domestic ones.
adapt well to life in captivity. 2 They are endemic animals from Brazil, The conditions that the animals are put through by the traffic greatly
being found in the Amazon forest, southeast and northeast of Brazil.3 deteriorate their health, as they are kept in tight places, without ventila-
tion and without access to water or food until they reach their final des-
Institution in which work was performed: Laboratory of Morphological Research, Federal tination. During this process, many of the animals die and others, when
University of Campina Grande – Patos, PB, Brazil


© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

J. Med. Primatol.. 2020;00:1–5. wileyonlinelibrary.com/journal/jmp | 1

, 2 | de SOUZA et Al.


apprehended by agents from the Brazilian Institute for the Environment IBAMA in the city of Cabedelo, Paraíba, Brazil—were used at
and Renewable Natural Resources (IBAMA) and sent to the Wild Animal the Veterinary Anatomy Laboratory, from the Health Center and
Screening Centers (CETAS), require veterinary medical care.4 Rural Technology, Federal University of Campina Grande (LAV/
One of the main systems of the animal organism frequently CSTR/UFCG). The project was submitted to the Research Ethics
affected in primates is the respiratory system, which is extremely Committee on the Use of Animals (CEUA) from the CSTR/UFCG
5
important for the maintenance of life, and several pathologies can and approved under protocol CEAU no. 59/2017 and to the
affect this system, such as, infectious inflammatory diseases or not, Authorization and Information and Biodiversity System (SISBIO)
neoplasms, dental diseases, trauma, parasitic diseases, all of which under no. 44489-1.
can cause changes in the respiratory system.6 The knowledge of the For the radiographic study of the paranasal sinuses, the carcasses
paranasal sinuses and the nasal cavity, in addition to their variations, were previously thawed and taken to the Diagnostic Imaging sector
is of great importance for the diagnosis of pathologies such as rhi- at the Veterinary Hospital Professor Ivon Macêdo Tabosa, from the
nosinusitis for example, and for surgical access of these structures Federal University of Campina Grande, Rural Health and Technology
in human medicine,7 and may be applied to veterinary medicine. Center, Campus of Patos, Paraíba, Brazil (HV/UFCG/CSTR). The po-
Knowledge about the relationship between the paranasal sinuses sitions used were adapted from what is routinely used for humans,
and the skull and its morphological variations are of great importance given the greater similarity between common marmosets and human
for understanding the function of this structure,8 as there are still dis- primates than with domestic animals. Radiographs were taken with
agreements among several authors about the real function that the two panoramic views: profile and frontal-naso, according to the
paranasal sinuses develop in the animal organism, as well as there is methodology by Rosa et al.14
still uncertain point about the development of pneumatization in the After the radiographs, the carcasses of the animals were taken to
facial skeleton.9 And, when compared to Old World primates, there the LAV/CSTR/UFCG for fixation and conservation in a 10% form-
are a lower number of studies that seek to bring information about aldehyde solution. To view the paranasal sinuses, paramedian and
10
the paranasal sinuses of New World primates. The studies carried transverse sections were made using a scalpel, anatomical forceps
out with paranasal sinuses of platyrrhini primates have the potential and a goldsmith saw. In order to identify the ethmoid sinus, which
to help in the search for knowledge about the function of the sinuses was not possible to be viewed macroscopically after the cuts, the his-
due to the great morphological variation found in the several species tological processing and cross-sectional serial cuts of the skull of the
11
of this group, acting as a natural experiment. C jacchus specimens were performed. To make the slides, an animal
Imaging examinations of the paranasal sinuses can help in the that was fixed in 10% formaldehyde was used, its head was disarticu-
identification and knowledge of the extent of morphological varia- lated, and dissected in order to remove the skin, muscles, and fascia.
tions, bone changes, or the presence of ectopic soft tissues.12 The The skull was washed in running water for fifteen minutes to remove
radiographic diagnostic method is widely used within veterinary excess of formaldehyde and then subjected to a descaling process
medicine because it has several advantages, such as the bene- with 5% nitric acid for 5 days. The nitric acid solution was changed
fit-cost ratio, being one of the most important diagnostic methods daily until complete descaling was obtained, confirmed by inserting a
for identifying various conditions that affect animals, however, so needle directly into one of the bones, so that it was then possible to
that the greatest benefit from this tool is achieved, it is necessary make the cuts for histological slides. After the 5 days of the descaling
the best application of specific techniques in order to obtain a su- process, the skull was removed from the acidic solution and washed
perior quality image.13 Despite the increase in the use of more with running water for 15 minutes, then the step of paraffin embed-
advanced techniques such as computed tomography in several ding and histological processing began. Serial 3-mm cuts were made
institutions, in Brazil, it has not yet become a widely accessible in the craniocaudal direction. The samples were processed routinely,
technique for use in wild animals, either due to the higher cost or included in paraffin, cut to 5 µm and stained with hematoxylin and
the unavailability of equipment in several regions, making it neces- eosin (HE). Histological processing was performed at the LAV/CSTR/
sary to resort to often to the use of conventional or computerized UFCG and in the Histopathology sector of the HV/UFCG/CSTR.
radiographs, which can be used as screening tests and which will
facilitate in a better direction of diagnosis or for the performance
of other complementary tests, when available. 3 | R E S U LT S
Therefore, our objective with this study was to identify the anat-
omy of the paranasal sinuses and define the incidence plans for ra- The frontal recess presented narrow cavities, not extending very
diographic examinations in common marmosets. caudally, remaining only in the most rostral third of the frontal bone,
without identifiable communication in the anatomical study with the
nasal cavity (Figure 1). The sphenoid paranasal sinuses are located
2 | M ATE R I A L A N D M E TH O DS in the body of the sphenoid bone and two cavities separated by a
septum could be identified, one more cranial and one more caudal,
Ten carcasses of common marmosets (C jacchus)—adults, com- being shown in Figure 1 this sinus in its rostrocaudal extension after
posed of five females and five males donated by the CETAS/ paramedian section of the skull.

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