cross-sectional anatomy, computed tomography and magnetic resonance imaging of the head of common...
TRANSCRIPT
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
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.
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
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.
(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
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.
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
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.
References
Amundin, M., and T. W. Cranford, 1990: Forehead anatomy
of Phocoena phocoena and Cephalorhynchus commersoni:
3-Dimensional computer generated reconstructions with
emphasis on the nasal diverticula. In: Sensory Abilities of
Cetacea: Laboratory and Field Evidence. (J. A. Thomas and
R. Kastelein, eds). New York: Plenum Press. pp 1–18.
Arencibia, A., J. M. V�azquez, M. Rivero, R. Latorre, J. A.
Sandoval, J. M. Vilar, and J. A. Ram�ırez, 2000: Computed
tomography of normal cranioencephalic structures in two
horses. Anat. Histol. Embryol. 29, 295–299.
Arencibia, A., M. A. Rivero, I. De Miguel, S. Contreras, A.
Cabrero, and J. Or�os, 2006: Computed tomographic anat-
omy of the head of the loggerhead sea turtle (Caretta caret-
ta). Res. Vet. Sci. 81, 165–169.
Asshauer, J., and M. Sager, 1997: MRI and CT Atlas of the
Dog. Berlin & London: Blackwell Science.
Besenski, N., 2002: Traumatic injuries: imaging of head inju-
ries. Eur. Radiol. 12, 1237–1252.
Bottcher, P., J. Maierl, T. Schiemann, C. Glaser, R. Weller, K.
H. Hoehne, M. Reiser, and H. G. Liebich, 1999: The visible
animal project: a three-dimensional, digital database for
high quality three-dimensional reconstructions. Vet. Radiol.
Ultrasound 40, 611–616.
Cranford, T. W., M. Amundin, and K. S. Norris, 1996: Func-
tional morphology and homology in the odontocete nasal
complex: implications for sound generation. J. Morphol.
228, 223–285.
Cranford, T. W., P. Krysl, and M. Amundin, 2010: A new
acoustic portal into the odontocete ear and vibrational
analysis of the tympanoperiotic complex. PLoS ONE 5,
e11927. doi:10.1371/journal.pone.0011927
De Rycke, L. M., J. H. Saunders, I. M. Gielen, H. J. van Bree,
and P. J. Simoens, 2003: Magnetic resonance imaging, com-
puted tomography, and cross-sectional views of the anatomy
of normal nasal cavities and paranasal sinuses in mesatice-
phalic dogs. Am. J. Vet. Res. 64, 1093–1098.
De Rycke, L. M., I. M. Gielen, S. A. Van Meervenne, P. J.
Simoens, and H. J. van Bree, 2005: Computed tomography
and cross-sectional anatomy of the brain in clinically normal
dogs. Am. J. Vet. Res. 66, 1743–1756.
Dennison, S. E., and T. Schwarz, 2008: Computed tomo-
graphic imaging of the normal immature California sea
lion head (Zalophus californianus). Vet. Radiol. Ultrasound
49, 557–563.
Feeney, D. A., T. F., Fletcher, and R. M.,Hardy 1991: Atlas of
Correlative Imaging Anatomy of the Normal Dog. Ultra-
sound and Computed Tomography. Philadelphia: W.B.
Saunders Company.
George, T. F., and J. E. Smallwood, 1992: Anatomic atlas for
computed tomography in the mesaticephalic dog: head and
neck. Vet. Radiol. Ultrasound 33, 217–240.
Hosokawa, H., and T. Kamiya, 1965: Sections of the dolphin’s
head (Stenella coeruleoalba). Sci. Rep. Whales Res. Inst. 19,
105–133.
Houser, D. S., J. Finneran, D. Carder, W. van Bonn, C. Smith,
C. Hoh, R. Mattrey, and S. Ridgway, 2004: Structural and
functional imaging of bottlenose dolphin (Tursiops trunca-
tus) cranial anatomy. J. Exp. Biol. 207, 3657–3665.
Kuiken, T. 1996: Diagnosis of By-Catch in Cetaceans. Euro-
pean Cetacean Society newsletter 26-special issue.
Liste, F., J. Palacio, V. Ribes, A. Alvarez-Clau, L. F. Domin-
guez, and J. M. Corpa, 2006: Anatomic and computed
tomographic atlas of the head of the newborn bottlenose
dolphin (Tursiops truncatus). Vet. Radiol. Ultrasound 47,
453–460.
Marino, L., T. L. Murphy, L. Gozal, and J. I. Johnson, 2001:
Magnetic resonance imaging and three-dimensional recon-
structions of the brain of a fetal common dolphin Delphinus
delphis. Anat. Embryol. 203, 393–402.
Marino, L., K. Sudheimer, D. A. Pabst, W. A. McLellan, D.
Filsoof, and J. I. Johnson, 2002: Neuroanatomy of the com-
mon dolphin (Delphinus delphis) as revealed by Magnetic
Resonance Imaging (MRI). Anat. Rec. 268, 411–429.
McKenna, M. F., J. A. Goldbogen, J. St Leger, J. A. Hilde-
brand, and T. W. Cranford, 2007: Evaluation of postmortem
changes in tissue structure in the bottlenose dolphin (Tursi-
ops truncatus). Anat. Rec. 290, 1023–1032.
Montie, E. W., G. E. Schneider, D. R. Ketten, L. Marino, K. E.
Touhey, and M. E. Hahn, 2007: Neuroanatomy of the suba-
dult and fetal brain of the Atlantic white-sided dolphin (La-
genorhynchus acutus) from in situ magnetic resonance
images. Anat. Rec. 290, 1459–1479.
Montie, E. W., G. E. Schneider, D. R. Ketten, L. Marino, K. E.
Touhey, and M. E. Hahn, 2008: Volumetric neuroimaging
of the brain of the Atlantic white-sided dolphin (Lagen-
orhynchus acutus). Anat. Rec. 291, 263–282.
Montie, E. W., C. A. Manire, and D. A. Mann, 2011: Live CT
imaging of sound reception anatomy and hearing measure-
ments in the pygmy killer whale, Feresa attenuata. J. Exp.
Biol. 214, 945–955.
Nomina Anatomica Veterinaria, 5th edn., 2005: Hannover,
Columbia-Missouri, Gent, Sapporo: World Association of
Veterinary Anatomists.
© 2014 Blackwell Verlag GmbH
Anat. Histol. Embryol.8
Sectional Anatomy and Imaging of Dolphin Head J. M. Alonso-Farr�e et al.
Oelschl€ager, H. H. A., M. Haas-Rioth, C. Fung, S. H. Ridgway,
and M. Knauth, 2008: Morphology and evolutionary biology
of the dolphin (Delphinus sp.) Brain-MR imaging and con-
ventional histology. Brain Behav. Evolut. 71, 68–86.
Oelschl€ager, H. H. A., S. H. Ridgway, and M. Knauth, 2010:
Cetacean Brain Evolution: Dwarf Sperm Whale (Kogia sima)
and Common Dolphin (Delphinus delphis) - an investigation
with high-resolution 3D MRI. Brain Behav. Evolut. 75, 33–62.
Rauschmann, M. A., S. Huggenberger, L. S. Kossatz, and H.
H. Oelschl€ager, 2006: Head morphology in perinatal dol-
phins: a window into phylogeny and ontogeny. J. Morphol.
267, 1295–1315.
Ridgway, S. H., L. Marino, and T. P. Lipscomb, 2002: Descrip-
tion of a poorly differentiated carcinoma within the brain-
stem of a White Whale (Delphinapterus leucas) from
magnetic resonance images and histological analysis. Anat.
Rec. 268, 441–449.
Ridgway, S., D. Houser, J. Finneran, D. Carder, M. Keogh, W.
Van Bonn, C. Smith, M. Scadeng, D. Dubowitz, R. Mattrey,
and C. Hoh, 2006: Functional imaging of dolphin brain
metabolism and blood flow. J. Exp. Biol. 209, 2902–2910.
Smallwood, J. E., B. C. Wood, W. E. Taylor, and L. P. Tate,
2002: Anatomic reference for computed tomography of the
head of the foal. Vet. Radiol. Ultrasound 43, 99–117.
Soldevilla, M. S., M. F. McKenna, S. M. Wiggins, R. E. Shad-
wick, T. W. Cranford, and J. A. Hildebrand, 2005: Cuvier’s
beaked whale (Ziphius cavirostris) head tissues: physical
properties and CT imaging. J. Exp. Biol. 208, 2319–2332.
Van Bonn, W., E., Jensen, and F.,Brook, 2001: Radiology,
computed tomography, and magnetic resonance imaging.
In: CRC Handbook of Marine Mammal Medicine, 2nd edn.
(L. A. Dierauf and F. M. D. Gulland, eds). Boca Raton,
Florida: CRC Press Inc., pp. 557–591.
Van Caelenberg, A. I., L. De Rycke, K. Hermans, L. Verhaert,
H. J. van Bree, and I. M. Gielen, 2010: Computed tomogra-
phy and cross-sectional anatomy of the head in healthy rab-
bits. Am. J. Vet. Res. 71, 293–303.
Van Caelenberg, A. I., L. De Rycke, K. Hermans, L. Verhaert,
H. J. van Bree, and I. M. Gielen, 2011: Low-field magnetic
resonance imaging and cross-sectional anatomy of the rabbit
head. Vet. J. 188, 83–91.
Zucca, P., G., Di Guardo, R., Pozzi-Mucelli, D., Scaravelli, and
M., Francese, 2004: Use of computer tomography for imag-
ing of Crassicauda grampicola in a Risso’s dolphin. J. Zoo
Wildl. Med. 35, 391–394.
© 2014 Blackwell Verlag GmbH
Anat. Histol. Embryol. 9
J. M. Alonso-Farr�e et al. Sectional Anatomy and Imaging of Dolphin Head