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ORIGINAL ARTICLE Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin (Delphinus delphis) and Striped Dolphin (Stenella coeruleoalba) J. M. Alonso-Farr e 1,2 *, M. Gonzalo-Orden 3 , J. D. Barreiro-V azquez 4 , A. Barreiro-Lois 4 , M. Andr e 5 , M. Morell 5 , M. Llarena-Reino 1,6 , T. Monreal-Pawlowsky 2 and E. Degollada 7 Addresses of authors: 1 Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universit ario de Santiago, 3810- 193, Aveiro, Portugal; 2 Parc Zool ogic de Barcelona, Parc de la Ciutadella s/n, 08003, Barcelona, Spain; 3 Faculty of Veterinary, Department of Animal Medicine, Surgery and Anatomy, University of Le on, Campus de Verganzana, 24071, Le on, Spain; 4 Imaging Diagnosis Service, Faculty of Veterinary, Department of Veterinary Clinical Science, University Veterinary Hospital Rof Codina, University of Santiago de Compostela, Avda.Carballo Calero s/n, 27002 Lugo, Spain; 5 Laboratory of Applied Bioacoustics, Politechnical University of Catalunya (LAB-UPC), Centre Tecnol ogic de Vilanova i la Geltr u, Avda. Rambla Ex- posici o s/n, 08800 Vilanova i la Geltr u, Barcelona, Spain; 6 ECOBIOMAR, Institute of Marine Research, (IIM-CSIC), C/Eduardo Cabello 6, 36208 Vigo, Spain; 7 Faculty of Veterinary, EDMAKTUB-Department of Anatomy and Embriology, Autonomous University of Barcelona, Edifici V, Campus UAB, 08193 Bellaterra, Spain *Correspondence Tel.: 0034932256780; fax: 0034932213853; e-mail: [email protected] With 12 figures Received July 2013; accepted for publication January 2014 doi: 10.1111/ahe.12103 Summary Computed tomography (CT) and low-field magnetic resonance imaging (MRI) were used to scan seven by-caught dolphin cadavers, belonging to two species: four common dolphins (Delphinus delphis) and three striped dolphins (Stenella coeruleoalba). CT and MRI were obtained with the animals in ventral recum- bency. After the imaging procedures, six dolphins were frozen at 20°C and sliced in the same position they were examined. Not only CT and MRI scans, but also cross sections of the heads were obtained in three body planes: trans- verse (slices of 1 cm thickness) in three dolphins, sagittal (5 cm thickness) in two dolphins and dorsal (5 cm thickness) in two dolphins. Relevant anatomical structures were identified and labelled on each cross section, obtaining a com- prehensive bi-dimensional topographical anatomy guide of the main features of the common and the striped dolphin head. Furthermore, the anatomical cross sections were compared with their corresponding CT and MRI images, allowing an imaging identification of most of the anatomical features. CT scans produced an excellent definition of the bony and air-filled structures, while MRI allowed us to successfully identify most of the soft tissue structures in the dolphin’s head. This paper provides a detailed anatomical description of the head structures of common and striped dolphins and compares anatomical cross sections with CT and MRI scans, becoming a reference guide for the interpretation of imaging studies. Introduction Computed tomography (CT) and magnetic resonance imaging (MRI) are non-invasive imaging techniques that are increasingly being used for anatomical descriptions, morphological studies and pathological diagnostics in marine mammals, mainly in cadavers (Van Bonn et al., 2001). The development and use of these techniques have revolutionized human and veterinary diagnostic proce- dures, allowing new ways to observe internal animal © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 1 Anatomia, Histologia, Embryologia

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Page 1: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

ORIGINAL ARTICLE

Cross-sectional Anatomy, Computed Tomography andMagnetic Resonance Imaging of the Head of CommonDolphin (Delphinus delphis) and Striped Dolphin (Stenellacoeruleoalba)J. M. Alonso-Farr�e1,2*, M. Gonzalo-Orden3, J. D. Barreiro-V�azquez4, A. Barreiro-Lois4, M. Andr�e5,M. Morell5, M. Llarena-Reino1,6, T. Monreal-Pawlowsky2 and E. Degollada7

Addresses of authors: 1 Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universit�ario de Santiago, 3810-

193, Aveiro, Portugal;2 Parc Zool�ogic de Barcelona, Parc de la Ciutadella s/n, 08003, Barcelona, Spain;3 Faculty of Veterinary, Department of Animal Medicine, Surgery and Anatomy, University of Le�on, Campus de Verganzana, 24071, Le�on, Spain;4 Imaging Diagnosis Service, Faculty of Veterinary, Department of Veterinary Clinical Science, University Veterinary Hospital Rof Codina, University

of Santiago de Compostela, Avda.Carballo Calero s/n, 27002 Lugo, Spain;5 Laboratory of Applied Bioacoustics, Politechnical University of Catalunya (LAB-UPC), Centre Tecnol�ogic de Vilanova i la Geltr�u, Avda. Rambla Ex-

posici�o s/n, 08800 Vilanova i la Geltr�u, Barcelona, Spain;6 ECOBIOMAR, Institute of Marine Research, (IIM-CSIC), C/Eduardo Cabello 6, 36208 Vigo, Spain;7 Faculty of Veterinary, EDMAKTUB-Department of Anatomy and Embriology, Autonomous University of Barcelona, Edifici V, Campus UAB,

08193 Bellaterra, Spain

*Correspondence

Tel.: 0034932256780;

fax: 0034932213853;

e-mail: [email protected]

With 12 figures

Received July 2013; accepted for publication

January 2014

doi: 10.1111/ahe.12103

Summary

Computed tomography (CT) and low-field magnetic resonance imaging (MRI)

were used to scan seven by-caught dolphin cadavers, belonging to two species:

four common dolphins (Delphinus delphis) and three striped dolphins (Stenella

coeruleoalba). CT and MRI were obtained with the animals in ventral recum-

bency. After the imaging procedures, six dolphins were frozen at �20°C and

sliced in the same position they were examined. Not only CT and MRI scans,

but also cross sections of the heads were obtained in three body planes: trans-

verse (slices of 1 cm thickness) in three dolphins, sagittal (5 cm thickness) in

two dolphins and dorsal (5 cm thickness) in two dolphins. Relevant anatomical

structures were identified and labelled on each cross section, obtaining a com-

prehensive bi-dimensional topographical anatomy guide of the main features

of the common and the striped dolphin head. Furthermore, the anatomical

cross sections were compared with their corresponding CT and MRI images,

allowing an imaging identification of most of the anatomical features. CT scans

produced an excellent definition of the bony and air-filled structures, while

MRI allowed us to successfully identify most of the soft tissue structures in the

dolphin’s head. This paper provides a detailed anatomical description of the

head structures of common and striped dolphins and compares anatomical

cross sections with CT and MRI scans, becoming a reference guide for the

interpretation of imaging studies.

Introduction

Computed tomography (CT) and magnetic resonance

imaging (MRI) are non-invasive imaging techniques that

are increasingly being used for anatomical descriptions,

morphological studies and pathological diagnostics in

marine mammals, mainly in cadavers (Van Bonn et al.,

2001). The development and use of these techniques have

revolutionized human and veterinary diagnostic proce-

dures, allowing new ways to observe internal animal

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol. 1

Anatomia, Histologia, Embryologia

Page 2: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

organs, and nowadays, CT and MRI are considered essen-

tial for the evaluation of normal and pathological condi-

tions of cephalic structures (Besenski, 2002).

Furthermore, a deep knowledge of the topographical

anatomy in a bi-dimensional plane can be regarded as the

key point to accurately interpret CT and MRI scans

(Bottcher et al., 1999). Several comparative studies

between CT and/or MRI and cross-sectional anatomy of

the head have been published on various terrestrial and

marine species, including dogs (Feeney et al., 1991;

George and Smallwood, 1992; Asshauer and Sager, 1997;

De Rycke et al., 2003, 2005), horses (Arencibia et al.,

2000), foals (Smallwood et al., 2002), rabbits (Van Cae-

lenberg et al., 2010, 2011), loggerhead sea turtles (Arenci-

bia et al., 2006), California sea lions (Dennison and

Schwarz, 2008) and also a comparison between CT and

corresponding cross sections of the head of a newborn

bottlenose dolphin (Liste et al., 2006). To the best of our

knowledge, the imaging and cryosectioning study of the

head of a perinatal pantropical spotted dolphin (Stenella

attenuata) by Rauschmann et al. (2006) is the only com-

parison between anatomical cross sections and CT and

MRI scans that can be found in the scientific literature.

The purpose of this study was to produce a complete

atlas of the bi-dimensional anatomy of the dolphin’s

head. The aim was also to compare anatomical cross sec-

tions and corresponding CT and MRI scans, in order to

provide a valuable tool to clinicians and researchers deal-

ing with dolphin species.

Materials and Methods

Seven dolphin cadavers belonging to two different spe-

cies were included in this study: four common dolphins

(Delphinus delphis) and 3 striped dolphins (Stenella co-

eruleoalba). The common dolphin specimens were 3

males and 1 female, ranging from 150 to 191 cm of

total length. The striped dolphin specimens were two

males and one female with body lengths ranging from

142 to 174 cm. All dolphins were found dead, inciden-

tally caught in fishing nets in NW Iberian Peninsula

(Spain and Portugal). All were selected by the technical

staff of the stranding networks (Coordinadora para o Es-

tudio dos Mam�ıferos Mari~nos-CEMMA in Spain and So-

ciedade Portuguesa de Vida Selvagem-SPVS in Portugal)

based on the lack of external evidences of disease and

fresh condition of the cadavers, considered to be <24 h

since the time of death. The dolphins were frozen

(�22°C) until the imaging examinations could be car-

ried out. The ethical committees of both institutions

approved the use of the cadavers for this study.

Magnetic resonance imaging examinations were per-

formed using a 0.2 Tesla MRI scanner (Signa Profile HD,

General Electrics Healthcare, Chalfont St. Giles, Bucking-

hamshire, UK) located at the veterinary faculty of Le�on

(Spain). A whole-body antenna was used to receive the

signal using Fast Recovery Spin Echo sequences in T1-

and T2-weighted modes (T1W and T2W) with a FOV of

28, as well as short pulse repetition time (TR) and echo

time (TE). Slice thickness and spacing were 4.0 mm and

1.2 mm, respectively, and the image acquisition matrix

was 512 9 512. MRI scans in transverse, sagittal and dor-

sal planes were obtained. CT scans were acquired with a

16-slice multirow helical CT scanner (ECLOS, Hitachi

Medical Systems Europe, Zug, Switzerland) and a work

station equipped with the KDS software (Kanteron Sys-

tems, New York, NY, USA), at the veterinary faculty of

Lugo (Spain). As a general protocol, CT scans were

obtained in transverse scans 1 mm thickness. Sagittal and

dorsal planes were examined from the software image

analysis. Two settings (soft tissues and bony tissues) were

used during CT scanning. During MRI and CT examina-

tions, the dolphins were completely thawed and placed in

ventral recumbency position.

After imaging, one striped dolphin was fully necropsied

due to the impossibility of it being frozen again. The

remaining 6 specimens were refrozen preserving the same

ventral recumbency position. These dolphins were cross-

sectioned using an electrical band saw along the trans-

verse plane at 1-cm intervals (two common dolphins),

along the sagittal plane (two common dolphins) and the

dorsal plane (two striped dolphins) at 5-cm intervals.

Slices were numbered, cleaned and photographed on both

sides. From these, we described the anatomical features of

the head, from the rostrum to the beginning of the spinal

cord. For each slice, corresponding and adjacent CT and

MRI scans were chosen trying to identify the best ana-

tomical correlation. Due to the impossibility of including

all cross sections, CT and MRI scans, only 11 slicing lev-

els were selected. Lines corresponding to these levels were

superimposed on a 3-D reconstruction of the head of an

adult male common dolphin (Fig. 1) and numbered

according the following figures. Figures 2–10 were correl-

atively presented from rostral to caudal orientation and

were labelled on the caudal surface, and therefore, they

show the right side of the dolphin to the right side of the

viewer. Anatomical structures that could be identified in

the cross sections were labelled according to the existing

cross-section studies of the dolphin’s cephalic region,

referred to the whole head (Hosokawa and Kamiya, 1965)

or the central nervous system (Oelschl€ager et al., 2008,

2010). The MRI data sets of the brain were also com-

pared with the in situ MRI study by Montie et al. (2007).

Structures not described in previous works were labelled

in accordance with the official anatomical terminology by

the Nomina Anatomica Veterinaria (2005).

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol.2

Sectional Anatomy and Imaging of Dolphin Head J. M. Alonso-Farr�e et al.

Page 3: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

Results

Results of the study are shown in Figs 1–12. All clinicallyrelevant structures of the dolphin’s head were identified

on cross sections. Not all the anatomical structures iden-

tified on cross sections were identified on CT and MRI

scans and vice versa. The cephalic anatomical features of

the common and the striped dolphin cross sections

appeared to be quite similar and subsequent comparisons

between sections, CT and MRI of both species were con-

sidered indistinguishable.

Magnetic resonance imaging scans have allowed to

successfully identify most of the soft tissue structures of

the dolphin’s head, including the differentiation of grey

(a) (b)

Fig. 1. Frontal (a) and lateral (b) views of

three-dimensional reconstructions of an adult

male common dolphin head from computed

tomography (CT) scans, indicating approxi-

mate levels of sections, CT and magnetic res-

onance imaging included in the Figs 2–12.

(a) (b) (c)

Fig. 2. Photograph of an anatomical transverse cross section (a), computed tomography image (b) and magnetic resonance imaging T2-weighted

image (c) of the head of a subadult common dolphin at the level of the rostral portion of the melon, corresponding to line 2 in Fig. 1b. The right

side of the head is oriented to the right of the images, and the ventral aspect of the head is oriented to the bottom of the images. 1 = Blubber.

2 = Mesorostral cartilage. 3 = Maxillary bone. 4 = Paraotic palatine sinus. 5 = Oral cavity. 6 = Tongue musculature. 7 = Mandible. 8 = Teeth.

9 = Rostral medial muscle. 10 = Rostral lateral muscle. 11 = Maxillary bone (palatine process). 12 = Melon. 13 = Mandible acoustic path.

(a) (b) (c)

Fig. 3. Photograph of an anatomical transverse cross section (a), computed tomography image (b) and magnetic resonance imaging T1-weighted

image (c) of the head of a subadult common dolphin at the level of the labial commissure, corresponding to line 3 in Fig. 1b. 1 = Blubber.

2 = Rostral medial muscle. 3 = Rostral lateral muscle. 4 = Maxillary bone. 5 = Frontal bone. 6 = Premaxillary bone. 7 = Melon. 8 = Paraotic sinus.

9 = Mesorostral cartilage. 10 = Mandible. 11 = Labial commissure. 12 = Vomer bone. 13 = Pterygoid muscle. 14 = Pterygoid bone. 15 = Masse-

ter muscle. 16 = Tongue musculature. 17 = Nasal plug musculature. 18 = Oropharynx. 19 = Digastric muscle. 20 = Mandible acoustic path.

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol. 3

J. M. Alonso-Farr�e et al. Sectional Anatomy and Imaging of Dolphin Head

Page 4: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

and white matter structures in the brain, some cranial

nerves, the eye and associated tissues, the larynx com-

plex and other muscle, fat and connective tissue. Cere-

brospinal fluid was also clearly identified by means of

T2-weighted MRI showing a very hyperintense (white)

signal into the ventricles. Odontocete sonar system

acoustic paths are located in the melon and around the

mandibles, and formed by very low-density fat tissue

(a) (b) (c)

Fig. 4. Photograph of an anatomical transverse cross section (a), computed tomography image (b) and magnetic resonance imaging T1-weighted

image (c) of the head of a subadult common dolphin at the level of the nasal tract, corresponding to line 4 in Fig. 1b. 1 = Blubber. 2 = Muscula-

ture of external nasal sacs system. 3 = Melon acoustic path. 4 = Premaxillary bone. 5 = Maxillary bone. 6 = Paraotic ophthalmic sinus. 7 = Paraot-

ic maxillary sinus. 8 = Mesorostral cartilage. 9 = Nasal bony tract. 10 = Periocular musculature. 11 = Pterygoid muscle. 12 = Sclera.

13 = Mandible. 14 = Zygomatic arch (malar bone). 15 = Mandible acoustic path. 16 = Paraotic palatine sinus. 17 = Pharyngeal sphincter muscle.

18 = Oro-pharynx. 19 = Pterygoid bone. 20 = Lens. 21 = Nasofrontal nasal sac.

(a) (b) (c)

Fig. 5. Photograph of an anatomical transverse cross section (a), magnetic resonance imaging (MRI) T2-weighted (b) and MRI T1-weighted images

(c) of the head of a subadult common dolphin at the level of the eyes, corresponding to line 5 in Fig. 1b. 1 = Blubber. 2 = Musculature of exter-

nal nasal sacs system. 3 = Paraotic ophthalmic sinus. 4 = Sclera. 5 = Periocular musculature. 6 = Ophthalmic rete. 7 = Vitreous humour. 8 = Ret-

ina. 9 = Lens. 10 = Mandible. 11 = Mandible acoustic path. 12 = Oro-pharynx. 13 = Hyoid bones. 14 = Pterygoid muscle. 15 = Pharyngeal

sphincter muscle. 16 = Optic nerve. 17 = Cerebral grey matter. 18 = Cerebral white matter. 19 = Cerebral frontal lobe. 20 = Sulcus interlobularis.

21 = Paraotic pterygoid sinus. 22 = Right vestibular nasal sac. 23 = Nasofrontal sac. 24 = Nasal plug.

(a) (b) (c)

Fig. 6. Photograph of an anatomical transverse cross section (a), magnetic resonance imaging (MRI) T2-weighted (b) and MRI T1-weighted images

(c) of the head of a subadult common dolphin at the rostral level of the brain, corresponding to line 6 in Fig. 1b. 1 = Blubber. 2 = Epicranialis

muscle. 3 = Nasal bone. 4 = Cerebral grey matter. 5 = Cerebral white matter. 6 = Internal capsula. 7 = Putamen. 8 = Septum lucidum. 9 = Sul-

cus interlobularis. 10 = Right lateral ventricle. 11 = Dorsal sagittal sinus. 12 = Corpus callosum. 13 = Optic nerve. 14 = Basisphenoid bone.

15 = Paratic sinus. 16 = Temporal bone. 17 = Mandible. 18 = Mandible acoustic path. 19 = Larynx complex. 20 = Pharyngeal sphincter muscle.

21 = Stylohyal bone. 22 = Thyrohyal bone. 23 = Basihyal bone.

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol.4

Sectional Anatomy and Imaging of Dolphin Head J. M. Alonso-Farr�e et al.

Page 5: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

(Cranford et al., 1996). These acoustic paths were clearly

identified and defined by hyperintense MRI signals

(especially in T2W ones), allowing a morphological

approach to the study of sound transmission through

the head tissues. On the MRI images, most of the bony

structures were poorly defined because of their hypoin-

tense (black) image pattern. Despite of this, some hard

tissues such as the mandible could be well observed due

to the contrast between the osseous and the adjacent

soft tissue structures.

(a) (b) (c)

Fig. 7. Photograph of an anatomical transverse cross section (a), computed tomography (b) and magnetic resonance imaging T2-weighted images

(c) of the head of a subadult common dolphin at the level of the tympano-periotic complex, corresponding to line 7 in Fig. 1b. 1 = Blubber.

2 = Epicranialis muscle. 3 = Parietal bone. 4 = Dorsal sagittal sinus. 5 = Left lateral ventricle. 6 = Corpus callosum. 7 = Thalamus. 8 = Cerebral

aqueduct. 9 = Internal capsula. 10 = Inferior collicle. 11 = Interthalamic adhesion. 12 = Optic nerve. 13 = Temporal bone. 14 = Paraotic peribul-

lary sinus. 15 = Periotic bone. 16 = Tympanic bone (Bulla tympanica). 17 = Middle ear cavity. 18 = Thyrohyal bone. 19 = Stylohyal bone.

20 = Corniculate cartilage. 21 = Epiglottic cartilage. 22 = Laryngo-pharynx. 23 = Fat connection between mandible acoustic path and tympano-

periotic complex.

(a) (b) (c)

Fig. 8. Photograph of an anatomical transverse cross section (a), magnetic resonance imaging (MRI) T2-weighted (b) and MRI T1-weighted images

(c) of the head of a subadult common dolphin at the level of the larynx complex, corresponding to line 8 in Fig. 1b. The cross section is slightly

caudal by the right side. 1 = Blubber. 2 = Epicranialis muscle. 3 = Dorsal sagittal sinus. 4 = Tentorium membranosum. 5 = Right lateral ventricle.

6 = Thalamus. 7 = Periaqueductal grey matter. 8 = Cerebral aqueduct. 9 = Inferior collicle. 10 = Pons. 11 = Cerebellar lobe. 12 = Tympano-

periotic complex. 13 = Vestibulocochlear nerve (VIII cranial nerve). 14 = Corniculate cartilage (larynx). 15 = Epiglottic cartilage (larynx). 16 = Fat

connection between mandible acoustic path and tympano-periotic complex.

(a) (b) (c)

Fig. 9. Photograph of an anatomical transverse cross section (a) and magnetic resonance imaging T1-weighted images (c) of the head of a suba-

dult common dolphin, and computed tomography (CT) scan (b) of and adult striped dolphin, at the level of the cerebellum, corresponding to line

9 in Fig. 1b. The CT is slightly caudal to the level of 9a and 9c. 1 = Blubber. 2 = Cerebral lobe. 3 = Tentorium oseum. 4 = Vermis cerebella.

5 = Medulla oblongata. 6 = Cerebellar lobe. 7 = Basioccipital bone. 8 = Temporal bone. 9 = Paraotic peribullary sinus. 10 = Oesophagus.

11 = Larynx complex. 12 = Hyoid bones. 13 = Stylohyal bone. 14 = Thyrohyal bone. 15 = Basihyal bone.

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol. 5

J. M. Alonso-Farr�e et al. Sectional Anatomy and Imaging of Dolphin Head

Page 6: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

Computed tomography scans produced an excellent

definition of bony structures of the head such as the skull,

ear bones, maxilla, mandible and other hyperattenuating

hard tissues such as the eye crystalline or the teeth, all of

them appearing as very hyperdense (white) images. The

tympano-periotic complex was especially well defined due

to its high-attenuation features, but the small size of the

complex did not allow a clear image definition of internal

structures, for example the ossicles and semi-circular

canals. Air-filled structures, such as the paraotic sinuses,

the nasal passages and even the nasal sacs were also well

identified by CT, as very hypodense images. Soft tissues

could not be very well distinguished using this technique

due to their similar attenuating properties. However,

attenuation differences between fat and muscle allowed

the definition of mandible and melon acoustic paths.

Discussion

During ‘in vivo’ and ‘post-mortem’ diagnostic proce-

dures in cetaceans, it is particularly important to evaluate

(a) (b) (c)

Fig. 10. Photograph of an anatomical transverse cross section (a), computed tomography (b) and magnetic resonance imaging T2-weighted

images (c) of the head of a subadult common dolphin at the level of the occipital condyles, corresponding to line 10 in Fig. 1b. The cross section

is slightly caudal by the left side. 1 = Blubber. 2 = Semispinalis muscle. 3 = Multifidus muscle. 4 = Spinal cord. 5 = Right condyle (occipital bone).

6 = Atlas. 7 = Trachea. 8 = Oesophagus. 9 = Scapula. 10 = Humerus bone (head). 11 = Cranial insertion of the pectoral flipper. 12 = Right lung

(apical pole).

(a) (b)

(d)(c)

Fig. 11. Photograph of an anatomical dorsal cross section of the head

of a subadult striped dolphin (a) and magnetic resonance imaging T2-

weighted images (b) (c) (d) of a subadult common dolphin, at differ-

ent levels of the brain, corresponding to lines 11 in Fig. 1a. The right

side of the head is oriented to the right of the images, and the rostral

aspect of the head is oriented to the top of the images. 1 = Blubber.

2 = Nasal passage. 3 = Cerebral white matter. 4 = Cerebral grey mat-

ter. 5 = Thalamus. 6 = Right lateral ventricle. 7 = Vermis cerebella.

8 = Cerebellar lobe. 9 = Left lateral ventricle. 10 = Third ventricle.

11 = Medulla oblongata. 12 = Cerebral lobe. 13 = Melon acoustic

path. 14 = Melon. F: image artefact produced by tissues still frozen.

(a) (b)

Fig. 12. Photograph of an anatomical sagittal cross section (a), and

magnetic resonance imaging (MRI) T2-weighted image (b) of the head

of a subadult common dolphin at the level of the brain corresponding

to line 12 in Fig. 1a. Cross section is slightly lateral to the left from

the sagittal midline and MRI is at midline level. The rostral side of the

head is oriented to the left of the images, and the ventral aspect of

the head is oriented to the bottom of the images. 1 = Blubber.

2 = Blowhole. 3 = Nasal bone. 4 = Premaxillary bone. 5 = Nasal bony

tract. 6 = Nasal plug. 7 = Melon acoustic path. 8 = Elliptical fatty

bodies. 9 = Maxillary bone. 10 = Pterygoid bone. 11 = Paraotic ptery-

goid sinus. 12 = Pharyngeal sphincter muscle. 13 = Larynx complex.

14 = Trachea. 15 = Oesophagus. 16 = Occipital bone. 17 = Thala-

mus. 18 = Superior collicle. 19 = Cerebellar white matter. 20 = Cere-

bellar grey matter. 21 = Cerebellum. 22 = Pons. 23 = Optic nerve.

24 = Cerebral lobe. 25 = Corpus callosum. 26 = Spinal cord.

27 = Atlas. 28 = Multifidus muscle. 29 = Semispinalis muscle.

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol.6

Sectional Anatomy and Imaging of Dolphin Head J. M. Alonso-Farr�e et al.

Page 7: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

the cephalic region, which contains vital organs and sys-

tems such as the central nervous system, the ear and

the system of air cavities which constitutes the paraotic

sinuses. These structures have a potentially relevant

pathological significance in stranded cetaceans, for

example viral encephalitis, acoustic traumas and parasit-

ism, respectively. In live animals, most methods used to

evaluate pathological conditions in these organs and sys-

tems are indirect, unspecific or do not allow definitive

diagnostics.

In dead cetaceans, the opening of the cranial cavity to

explore the brain and the dissection of other cephalic

structures such as the ears or the paraotic sinuses are

complex and time-consuming procedures and imply

destruction of tissues. This often leads the technicians to

overlook these parts during the necropsy and conse-

quently miss lesions in these important areas. Complete

(macro and histological) evaluation of the head and

especially the ears has become very important in recent

years, especially looking into sonar system and blast

traumas. The acquisition and storage of CT/MRI data

sets from dolphin cadavers and the possibility of three-

dimensional reconstruction previous to the opening of

the carcasses could be considered a very useful tool to

look for some macroscopic lesions in certain anatomical

structures with a difficult access. Furthermore, they con-

siderably improve post-mortem information prior to dis-

section and allow re-examination of the cases even

many years after necropsy. Finally, imaging techniques

could be very valuable for gathering pathological, ana-

tomical and morphological data from museum speci-

mens or dolphins that cannot be fully necropsied,

although in any case, they cannot replace histology for

precise diagnostics.

Although post-mortem imaging morphology of dolphin

head tissues has correlated well with imaging of live tis-

sues (McKenna et al., 2007), it is essential to take into

account the possibility of decomposition artefacts which

typically appear when dealing with cadavers (e.g. gas for-

mation or tissue degradation). The extremely fresh condi-

tion of the dolphins included in the present study, the

fast freezing of the individuals after the stranding or by-

catch event, the good preservation conditions and finally

the slow thawing process of the carcasses just before the

CT and MRI examinations, allowed limiting these

artefacts. Additionally, the absence of diseases in a dead

cetacean is considered a possible indication of incidental

by-catch (Kuiken, 1996). As only by-caught dolphins

without external evidences of disease have been included

in this study, results could be considered suitable to

describe normality.

Due to the important variations in density among ana-

tomical structures, the cetacean cephalic region has

proved to be an excellent anatomical area to be exam-

ined through CT and MRI. The usefulness of these tech-

niques has been demonstrated in cetacean

neuroanatomical (Montie et al., 2007, 2008; Oelschl€ager

et al., 2008, 2010), functional (Amundin and Cranford,

1990; Houser et al., 2004; Soldevilla et al., 2005; Ridgway

et al., 2006; Cranford et al., 2010; Montie et al., 2011)

and pathological (Ridgway et al., 2002; Zucca et al.,

2004) research. Although MRI anatomical features of dif-

ferent cetacean species including the common dolphin

have been described from brains extracted from the skull

and fixed in formalin (Marino et al., 2001, 2002), the

procedures of removal and fixation may affect the spatial

relationships, the integrity and the dimensions of the

brain structures (Montie et al., 2007) and thus not allow-

ing a clinical or pathological use of the image data sets.

Detailed ‘in situ’ CT and MRI descriptions presented in

our work validate these imaging techniques for suitable

assessment of main internal tissues of the head. This vali-

dation could be extended to live dolphins, because our

image data set is consistent with the very few existing

peer-reviewed reports of live dolphin examinations

through CT (Houser et al., 2004; Montie et al., 2011)

and MRI (Ridgway et al., 2006). The use of CT and MRI

in dolphins is currently still very limited, but the interest

in moving forward in its use is considerable, especially

when dealing with endangered species because of the

amount of anatomical, pathological and morphological

information that these techniques provide in short image

acquisition times.

As described for other animal species, soft tissues,

organs and cavitary structures containing fluids showed

higher definition through MRI than CT. On the other

hand, CT provided better images of shapes and margins

of bony and gas-filled structures. The definition of CT

and MRI image patterns for most of the cephalic anatom-

ical structures has been successfully achieved, allowing

setting up of baseline data to identify and interpret

lesions. One of the main limitations for using these imag-

ing techniques for diagnostic purposes is the low image

resolution produced by small structures. However, as CT

and MRI equipments improve so will the image resolu-

tion of all structures.

This paper provides a comprehensive bi-dimensional

topographical anatomy atlas of the head of common and

striped dolphins, comprising macroscopic cross sections,

CT and MRI images, and should serve as a reference

guide for the interpretation of normal and pathological

imaging studies of this anatomical area. To our knowl-

edge, this is the first ‘Cross-section/CT/MRI’ cephalic

anatomy comparative atlas of these two dolphin species,

and it could be considered a suitable tool to clinicians

and researchers investigating dolphins.

© 2014 Blackwell Verlag GmbH

Anat. Histol. Embryol. 7

J. M. Alonso-Farr�e et al. Sectional Anatomy and Imaging of Dolphin Head

Page 8: Cross-sectional Anatomy, Computed Tomography and Magnetic Resonance Imaging of the Head of Common Dolphin ( Delphinus delphis ) and Striped Dolphin ( Stenella coeruleoalba )

Acknowledgements

The authors want to thank stranding networks staff of

Galicia (CEMMA) and Northern Portugal (SPVS) for

technical support to this research, especially to M. Ferre-

ira, J. Vingada, M. Caldas, JM. Cedeira, P. Covelo, JI.

D�ıaz, N. Alema~n and A. L�opez. The first author is cur-

rently funded by the post-doctoral fellowship SFRH/BPD/

47251/2008 of the Fundac�~ao para a Ciencia e a Tecnolo-

gia, Portugal.

Conflict of Interest

There are no conflict of interests.

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