Computed Tomography andCross-Sectional Anatomy of the

Thorax of the Live Bottlenose Dolphin(Tursiops truncatus)

MARINA IVAN�CIC,1* MAURICIO SOLANO,2 AND CYNTHIA R. SMITH1

1National Marine Mammal Foundation, San Diego, California2Cummings School of Veterinary Medicine, Tufts University,

North Grafton, Massachusetts

ABSTRACTPulmonary disease is one of the leading causes of cetacean morbidity

and mortality in the wild and in managed collections. The purpose of thisstudy was to present the computed tomographic (CT) appearance of thethorax of the live bottlenose dolphin (Tursiops truncatus) out-of-waterand to describe the technical and logistical parameters involved in CTimage acquisition in this species. Six thoracic CT evaluations of four con-scious adult bottlenose dolphins were performed between April 2007 andMay 2012. Animals were trained to slide out of the water onto foam padsand were transported in covered trucks to a human CT facility. Underlight sedation, animals were secured in sternal recumbency for acquisi-tion of CT data. Non-contrast helical images were obtained during anend-inspiratory breath hold. Diagnostic, high quality images wereobtained in all cases. Respiratory motion was largely insignificant due tothe species’ apneustic respiratory pattern. CT findings characteristic ofthis species include the presence of a bronchus trachealis, absence of lunglobation, cranial cervical extension of the lung, lack of conspicuity ofintrathoracic lymph nodes, and presence of retia mirabilia. Dorsoventralnarrowing of the heart relative to the thorax was seen in all animals andis suspected to be an artifact of gravity loading. Diagnostic thoracic com-puted tomography of live cetaceans is feasible and likely to prove clini-cally valuable. A detailed series of cross-sectional reference images isprovided. Anat Rec, 297:901–915, 2014. VC 2014 Wiley Periodicals, Inc.

Key words: anatomy; computed tomography; thorax; cetacean;dolphin; Tursiops truncatus

Pulmonary disease is one of the leading causes ofcetacean morbidity and mortality in the wild and inmanaged collections (Baker, 1992; DiGuardo et al., 1995;Harper et al., 2001; Miller et al., 2002; Bogomolni et al.,2010; Venn-Watson et al., 2012). For veterinarianscharged with the medical care of dolphins, prompt detec-tion of pulmonary abnormalities is imperative. This isparticularly true given that underlying pulmonary dis-ease can be clinically silent, and dolphins are adept atmasking illness (McBain, 2001).

Diagnostic imaging of the lungs of larger aquatic spe-cies using radiography and ultrasonography has been

Grant sponsor: Office of Naval Research; Grant number:N0001412WX20890; Grant sponsor: Navy Marine MammalProgram.

*Correspondence to: Marina Ivancic; National Marine Mam-mal Foundation, 2240 Shelter Island Drive, Suite 200, SanDiego, CA 92106. E-mail: marina.ivancic@nmmf.org

Received 31 March 2013; Accepted 7 January 2014.

DOI 10.1002/ar.22900Published online 4 March 2014 in Wiley Online Library(wileyonlinelibrary.com).

THE ANATOMICAL RECORD 297:901–915 (2014)

VVC 2014 WILEY PERIODICALS, INC.

reported (Van Bonn et al., 2001; Smith et al., 2012).These thoracic imaging techniques have inherent limita-tions and challenges. With radiography, the entirety ofthe lung cannot be evaluated in a single image. Eight toten sectional radiographs are commonly needed to evalu-ate the thorax in bottlenose dolphins, where the animalcan weigh more than 300 kg (Van Bonn et al., 2001). Inaddition, large patient size necessitates higher exposuresettings. Generators capable of producing X-rays power-ful enough to penetrate large animal patients are nottypically hand-held, and therefore not readily availablein the field (Pease, 2009). Further, radiography of thethorax requires a dolphin to be removed from the water.

Thoracic ultrasonography can be performed with thedolphin either in or out of the water, however only theperiphery of the thorax can be evaluated due to acousticshadowing from air-filled lung. Examination has provento be clinically valuable but is limited to the thoracicwall, intercostal muscles, pleural surface, and peripherallymph nodes in healthy animals (Smith et al., 2012).Deeper structures can be seen but require the presenceof peripheral lung consolidation or a mild to moderatevolume of pleural effusion (Rantanen, 1986; Reef et al.,1991; Tidwell, 1998; Reichle and Wisner, 2000). Acousticshadowing deep to each rib also limits evaluation. Thedepth of penetration of an ultrasound transducer is lim-ited by its wavelength, and wavelength is inversely pro-portional to frequency. The frequency of the transduceralso dictates the axial spatial resolution of the image(along the axis of the beam). Hence, in order to pene-trate deeper tissues in larger animals, transducers thatuse longer wavelengths and lower frequencies areneeded. This results in decreased spatial resolution(Rantanen, 1986; Reef et al., 1991).

Computed tomography (CT) is a cross-sectional diag-nostic imaging modality that allows detailed examina-tion of the entire thorax. This modality is notsusceptible to the intrinsic superimposition limitationsof radiography (Prather et al., 2005), or the acousticshadowing and depth limitations of ultrasonography.

TABLE 1. List of anatomical structures

1. Trachea2. Articulatio atlanto-occipitalis3. Lnn. cervicales superficiales4. Subdermal connective tissue sheath5. M. semispinalis6. M. longissimus7. Esophagus8. Basal cranial retia or cervical arterial retia9. Mm. multifidi

10. Vertebral body of fused atlas-axis(vertebrae cervicales I and II)

11. Right scapula12. Left scapula13. Right lung lobe14. Extremitas caudalis, vertebra cervicalis III15. Lamina arcus, vertebra cervicalis IV16. M. longus capitis17. Left lung lobe18. A. subclavia sinistra19. Vertebra cervicalis VII20. Right humerus21. Extremitas caudalis, vertebra thoracica I22. M. iliocostalis23. A. costocervicalis dextra24. V. brachiocephalica sinistra25. Truncus brachiocephalicus dexter26. Bronchus trachealis27. V. costocervicalis dextra28. Left humerus29. Extremitas cranialis, vertebra thoracica III30. Thoracic retia mirabilia31. Vena cava cranialis32. Sternum33. Costa asternalis sinistra III34. M. sternocephalicus35. Right radius36. Right ulna37. Vertebra thoracica IV38. Bifurcatio tracheae39. Aorta40. Arcus aortae41. Bronchus lobares of the bronchus trachealis42. Extremitas caudalis, vertebra thoracica IV43. Left radius44. Left ulna45. Bronchus segmentales of bronchus principalis sinister46. Bronchus principalis dexter (BPD)47. Bronchus principalis sinister (BPS)48. Processus articularis cranialis, vertebra thoracica V49. Articulatio capitis costae50. Junction, costa asternalis and costa sternalis51. Bronchus segmentales, BPS52. Vertebra thoracica V53. Atrium dextrum54. Vertebra thoracica VI55. Bronchus lobares of BPD56. Bronchus segmentales of BPD57. Bronchus segmentales of BPS58. Extremitas caudalis, vertebra thoracica VI59. Processus spinosus, vertebra thoracica VI60. Ventriculus dexter61. Vertebra thoracica VII62. Vena cava caudalis63. Extremitas cranialis, vertebra thoracica VIII64. Region of Lnn. marginales65. Vertebra thoracica VIII66. Bronchus segmentales of bronchus trachealis67. Vertebra thoracica IX68. Processus spinosus, vertebra thoracica VIII

TABLE 1. (continued)

69. Liver70. Vertebra thoracica X71. Extremitas caudalis, vertebra thoracica X72. Vertebra thoracica XI73. Extremitas caudalis, vertebra thoracica XI74. M. hypaxalis lumborum75. Region of fundic chamber76. M. rectus abdominis77. Gas in forestomach78. Gas in fundic chamber79. Vertebra thoracica XII80. Discus intervertebralis, vertebrae thoracicae

XII and XIII81. Vertebra thoracica XIII82. Fluid in forestomach83. Bronchus lobares, BPS84. M. sternohyoideus85. Heart86. A. pulmonalis dextra87. Costa sternalis88. A. pulmonalis sinistra89. V. pulmonalis dextra90. V. pulmonalis sinistra

902 IVAN�CIC ET AL.

Current CT technology can generate detailed thoracicimages with high tissue contrast resolution and onlyslightly decreased spatial resolution relative to digitalradiography. As multi-detector (multi-slice) CT scannersare becoming increasingly available (Habing et al., 2010;Drees et al., 2011), rapid assessment of large anatomicalregions is possible. This is of particular value in ceta-ceans, since sizeable volumes of tissue must be eval-uated while minimizing time on land. A number of

previous investigations have described cross-sectionaldiagnostic imaging in marine mammals, most recently ofthe thorax (Alonso-Farr�e et al., 2013), however with fewexceptions (Finneran, 2003; Dennison et al., 2009b; Mon-tie et al., 2011) nearly all of these studies have been per-formed post-mortem (Marino et al., 2001a, b, c, 2002,2003a, b, c, 2004a, b; Liste et al., 2006; Dennison andSchwarz, 2008; Ketten and Montie, 2008; Moore et al.,2009; Moore et al., 2011; Dennison et al., 2012; Alonso-Farr�e et al., 2013). Despite their important scientificvalue, their clinical applicability is limited.

Fig. 2. Lateral thoracic CT scout. Cranial is to the left of the image. Each numbered line indicates thelevel at which Figs. 3 through 25 were obtained. Vertebra thoracica I (T1), vertebra thoracica VII (T7), ver-tebra thoracica XII (T12), and vertebra lumbalis V (L5) are identified.

Fig. 1. A dolphin is seen positioned on the CT table in sternalrecumbency with tucked pectoral flippers, secured by table straps.Suction cup electrodes are in place to monitor ECG (electrocardiogra-phy) data; these are removed during image acquisition. Note that theanimal here is positioned in a tail-first orientation relative to the CTgantry. A head-first orientation is more commonly used when scanningthe thorax.

Fig. 3. Figures 3–25 include (A) a line drawing detailing anatomicalstructures, and three transverse CT images in (B) lung 1400/2500, (C)soft tissue 350/40, and (D) bone 1500/300 WW/WL (window width/window level). The right side of the animal is to the readers’ left in allimages. Figure number corresponds to the reference line number inFig. 2. 1. laryngeal-tracheal margin, 2. articulatio atlanto-occipitalis, 3.Lnn. cervicales superficiales, 4. subdermal connective tissue sheath,5. M. semispinalis cervicis, 6. M. longissimus cervicis, 84. M.sternohyoideus

BOTTLENOSE DOLPHIN THORACIC CT ANATOMY 903

The Navy Marine Mammal Program (MMP) firstbegan conducting CT evaluation of live dolphins in 2004(Houser et al., 2004). Since that time, CT has become an

indispensible diagnostic imaging modality for the MMP(Houser et al., 2010) in both screening for and monitor-ing pulmonary parenchymal abnormalities. The purpose

Fig. 4. 1. trachea, 4. subdermal connective tissue sheath, 5. M. semi-spinalis cervicis, 6. M. longissimus cervicis, 7. esophagus, 8. basal cra-nial retia or cervical arterial retia, 9. Mm. multifidi, 10. vertebral body offused atlas-axis (vertebrae cervicales I and II), 11. right scapula, 12. leftscapula, 13. cupula of right lung lobe, 84. M. sternohyoideus.

Fig. 5. 1. trachea, 4. subdermal connective tissue sheath, 5. M.semispinalis cervicis, 6. M. longissimus cervicis, 7. esophagus, 8.basal cranial retia or cervical arterial retia, 9. Mm. multifidi, 11. rightscapula, 12. left scapula, 13. cupula of right lung lobe, 14. extremitascaudalis, vertebra cervicalis III, 15. lamina arcus, vertebra cervicalis IV,16. M. longus colli, 84. M. sternohyoideus.

Fig. 6. 1. trachea, 4. subdermal connective tissue sheath, 7. esoph-agus, 8. basal cranial retia or cervical arterial retia, 9. Mm. multifidi,11. right scapula, 12. left scapula, 13. right lung lobe, 16. M. longuscapitis, 17. cupula of left lung lobe, 18. A. subclavia sinistra, 19. verte-bra cervicalis VII, 84. M. sternohyoideus.

Fig. 7. 1. trachea, 4. subdermal connective tissue sheath, 7. esopha-gus, 8. basal cranial retia or cervical arterial retia, 11. right scapula, 12. leftscapula, 13. right lung lobe, 16. M. longus capitis, 17. left lung lobe, 18. A.subclavia sinistra, 20. caput humerus dexter, 21. extremitas caudalis, ver-tebra thoracica I, 22. M. iliocostalis thoracis, 23. A. costocervicalis dextra,24. V. brachiocephalica sinistra, 25. truncus brachiocephalicus dexter.

904 IVAN�CIC ET AL.

of this study is to present the CT appearance of thethorax of the conscious, healthy bottlenose dolphin (Tur-siops truncatus) and to describe the logistics involved inCT image acquisition for this aquatic species. To ourknowledge, this is the first detailed anatomical report ofextra-cranial cross-sectional diagnostic imaging of a livemarine mammal species.

MATERIALS AND METHODS

Thoracic computed tomographic evaluations of fourhealthy live adult bottlenose dolphins were performedbetween April 2007 and May 2012. This included threemales and one female (age range, 11–28 years, mean16.8 years; weight range, 154–218 kg, mean 177 kg;length range, 244–264 cm, mean 251 cm). One animalwas evaluated on three separate occasions. All other ani-mals were evaluated once. At the time of each evalua-tion, individual animal measurements were as follows:Animal 1 5 264 cm total body length, 213–218 kg totalbody weight (varied across three scans); Animal 2 5 248cm total body length, 175 kg total body weight; Animal3 5 244 cm total body length, 154 kg total body weight;Animal 4 5 247 cm total body length, 163 kg total bodyweight (total body length here is defined as the distancefrom the tip of the rostrum to the caudal margin of the

Fig. 8. 1. trachea, 4. subdermal connective tissue sheath, 6. M.longissimus thoracis, 7. esophagus, 11. right scapula, 12. left scapula,13. right lung lobe, 17. left lung lobe, 18. A. subclavia sinistra, 20. righthumerus, 23. A. costocervicalis dextra, 25. truncus brachiocephalicusdexter, 26. bronchus trachealis, 27. V. costocervicalis dextra, 28. caputhumerus sinister, 29. extremitas cranialis, vertebra thoracica III, 30.thoracic retia mirabilia, 31. vena cava cranialis, 32. sternum, 33. costaasternalis sinistra III.

Fig. 9. 4. subdermal connective tissue sheath, 7. esophagus, 9. Mm.multifidi, 11. right scapula, 12. left scapula, 13. right lung lobe, 17. leftlung lobe, 28. left humerus, 30. thoracic retia mirabilia, 31. vena cavacranialis, 32. sternum, 34. M. sternocephalicus, 35. right radius, 36.right ulna, 37. vertebra thoracica IV, 38. bifurcatio tracheae, 39. aortaascendens, 40. arcus aortae, 41. bronchus lobares of the bronchustrachealis.

Fig. 10. 4. subdermal connective tissue sheath, 7. esophagus, 11.right scapula, 12. left scapula, 13. right lung lobe, 17. left lung lobe,31. vena cava cranialis, 32. sternum, 34. M. sternocephalicus, 35. rightradius, 36. right ulna, 39. aorta descendens, 42. extremitas caudalis,vertebra thoracica IV, 43. left radius, 44. left ulna, 45. bronchus seg-mentales of bronchus principalis sinister, 46. bronchus principalis dex-ter, 47. bronchus principalis sinister, 48. processus articularis cranialis,vertebra thoracica V, 49. articulatio capitis costae, 50. junction, costaasternalis and costa sternalis, 66. bronchus segmentales of bronchustrachealis, 85. heart. Note the asymmetrical appearance of the thoraxin this figure, as the animal is leaning to the left (right of the image).The external body wall has an angular contour dorsal to the left pecto-ral flipper and the left-sided ribs have a more angular appearance,consistent with some out-of-water thoracic collapse.

BOTTLENOSE DOLPHIN THORACIC CT ANATOMY 905

tail flukes on midline). None of the animals had clinicalevidence of thoracic disease or hematological or biochem-ical evidence of infection or inflammation.

The dolphins were removed from open ocean pens atthe MMP either by voluntarily beaching onto foam padsor by swimming into stretchers. One animal was pre-medicated with oral diazepam 0.13 mg/kg prior to beach-ing. The animals were transported 8.5 miles in coveredtrucks to a human medical facility. Veterinary personnelcontinuously monitored basic physiological parametersincluding heart rate, respiratory rate, and ECG (electro-cardiography). Light sedation was administered onarrival (0.02–0.09 mg/kg intramuscular midazolam inthe M. longissimus dorsi lateral to the dorsal fin). CTequipment was protected with plastic sheeting. The ani-mals were secured in sternal recumbency with tuckedpectoral flippers and transferred to the CT table using ahuman spine board (Fig. 1). Water was intermittentlyand judiciously misted onto the animals’ skin. Care wastaken in positioning the dolphins as upright as possibleto minimize atelectasis, undue pressure on the pectoralflippers, and image obliquity/asymmetry. CT evaluationof the thorax was performed by scanning from the occi-put to the mid-level of the dorsal fin in conjunction withother regions of clinical interest specific to each animal’smedical history (head, ears, kidneys, and/or humeraljoints).

Images were acquired using a multi-detector 16-slicehelical CT scanner with an 80 cm bore and 227 kg table

weight limit.1 Non-contrast CT images were obtainedopportunistically during an end-inspiratory breath-holdcharacteristic of cetaceans. Image acquisition was initi-ated immediately following inhalation, and the entireregion of interest was scanned during a single breath-hold. Technical parameters included a standard algo-rithm, 140 kVp (kilovolt potential) to minimize beamhardening, automatically generated mA (milliamperes)(range, 300–715), a rotational speed of 0.5 sec, and apitch of 1.75 to minimize scan time. Helical 1.25 mm sli-ces with data interpolation were obtained initially andretrospectively reconstructed to overlapping 1.25 mm 30.625 mm series in soft tissue, lung, and bone recon-struction algorithms.

The dolphins were immediately transported back toocean enclosures following the scan. A reversal agentwas administered (0.003–0.012 mg/kg flumazenil) eitherintravenously in the caudal peduncle periarterial venousrete, the ventral fluke periarterial venous rete, or intra-muscularly in the M. longissimus dorsi following threeof the six CT scans. This was given after departure fromthe human medical facility and prior to water re-entry.The average CT scan time was 50 min and the averageduration of time out of the water was 3 hr.

All thoracic CT studies were evaluated at the time ofimage acquisition for clinical purposes by the attendingveterinarian and retrospectively by a board-certified vet-erinary radiologist (MI) for the purpose of this publica-tion. Dedicated open-source DICOM (digital imaging

Fig. 11. 4. subdermal connective tissue sheath, 7. esophagus, 13.right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 32. ster-num, 34. M. sternocephalicus, 43. left radius, 44. left ulna, 46. bron-chus principalis dexter, 47. bronchus principalis sinister (BPS), 51.bronchus segmentales, BPS, 52. vertebra thoracica V, 53. atrium dex-trum, 85. Heart. Note the asymmetrical appearance of the thorax inthis figure, as the animal is leaning to the left (right of the image). Theexternal body wall has an angular contour dorsal to the left pectoralflipper and the left-sided ribs have a more angular appearance, con-sistent with some out-of-water thoracic collapse.

Fig. 12. 4. subdermal connective tissue sheath, 5. M. semispinalisthoracis, 6. M. longissimus thoracis, 7. esophagus, 9. Mm. multifidi, 13.right lung lobe, 17. left lung lobe, 22. M. iliocostalis thoracis, 32. sternum,34. M. sternocephalicus, 39. aorta descendens, 46. bronchus principalisdexter (BPD), 47. bronchus principalis sinister, 54. vertebra thoracica VI,55. bronchus lobares of BPD, 56. bronchus segmentales of BPD, 57.bronchus segmentales of BPS, 85. heart, 86. A. pulmonalis dextra.

1GE Lightspeed 16, General Electric Medical Systems, Fairfield,Connecticut

906 IVAN�CIC ET AL.

communications in medicine) viewing software2 was usedfor qualitative and quantitative image analysis. Linedrawings were created by hand-tracing each CT imagewith a computer mouse using commercially available illus-tration software.3 The line drawings were utilized to detailrelevant anatomy without compromising the quality of theCT images (Figs. 3–25). Anatomical references usedinclude anatomic texts and previously published atlases(Tyson, 1680; Hunter and Banks, 1787; Wilson, 1880;Wislocki, 1929; Wislocki, 1942; Wislocki and Belanger,1960; Nakajima, 1961; Boice et al., 1964; Hosokawa andKamiya, 1965; Galliano et al., 1966; Viamonte et al., 1969;Green, 1972; Smith et al., 1976; McFarland et al., 1979;Pabst, 1990; Rommel, 1990; Pabst, 1996; Kastelein et al.,1997; Melnikov, 1997; Harper et al., 2001; Rommel andLowenstine, 2001; Buchholtz and Schur, 2004; De Rykeet al., 2005; World Association of Veterinary Anatomists,2005; Rommel et al., 2006, 2007; Cooper et al., 2007; Cot-ten et al., 2008; Piscitelli et al., 2010; Costidis and Rom-mel, 2012). Mean values and standard deviations foranatomical measurements were calculated using an onlineopen-source statistics calculator.4

The MMP is accredited by the Association for Assess-ment and Accreditation of Laboratory Animal CareInternational and adheres to the national standards ofthe United States Public Health Service Policy on theHumane Care and Use of Laboratory Animals and theAnimal Welfare Act. As required by the Department of

Fig. 13. 4. subdermal connective tissue sheath, 7. esophagus, 9.Mm. multifidi, 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalisthoracis, 30. thoracic retia mirabilia, 32. sternum, 39. aorta descendens,46. bronchus principalis dexter (BPD), 47. bronchus principalis sinister(BPS), 51. bronchus segmentales, BPS, 56. bronchus segmentales,BPD, 58. extremitas caudalis, vertebra thoracica VI, 59. processus spi-nosus, vertebra thoracica VI, 60. ventriculus dexter, 85. heart, 86. A.pulmonalis dextra, 87. costa sternalis, 88. A. pulmonalis sinistra.

Fig. 14. 4. subdermal connective tissue sheath, 7. esophagus, 13.right lung lobe, 17. left lung lobe, 22. M. iliocostalis thoracis, 32. ster-num, 39. aorta descendens, 46. bronchus principalis dexter, 47. bron-chus principalis sinister, 61. vertebra thoracica VII, 62. vena cavacaudalis, 85. heart, 86. A. pulmonalis dextra, 87. costa sternalis, 88. A.pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

Fig. 15. 4. subdermal connective tissue sheath, 7. esophagus, 13.right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 39. aortadescendens, 46. bronchus principalis dexter, 47. bronchus principalissinister, 62. vena cava caudalis, 63. extremitas cranialis, vertebrathoracica VIII, 85. heart, 86. A. pulmonalis dextra, 88. A. pulmonalissinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

2Osirix 4.0, Pixmeo, Geneva, Switzerland3Adobe Illustrator CS6, Adobe Systems, San Jose, California4Standard Deviation Calculator. Web. 28 Feb, 2013. http://easy-

calculation.com/statistics/standard-deviation.php

BOTTLENOSE DOLPHIN THORACIC CT ANATOMY 907

Fig. 16. 4. subdermal connective tissue sheath, 7. esophagus, 13.right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 39. aortadescendens, 46. bronchus principalis dexter, 47. bronchus principalissinister (BPS), 49. articulatio capitis costae, 64. region of Lnn. margin-ales, 65. vertebra thoracica VIII, 83. bronchus lobares, BPS, 85. heart,86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pulmonalisdextra, 90. V. pulmonalis sinistra.

Fig. 17. 4. subdermal connective tissue sheath, 7. esophagus, 13.right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 39.aorta descendens, 46. bronchus principalis dexter, 47. bronchusprincipalis sinister, 67. vertebra thoracica IX, 68. processus spino-sus, vertebra thoracica VIII, 69. liver, 86. A. pulmonalis dextra, 88.A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalissinistra.

Fig. 18. 4. subdermal connective tissue sheath, 7. esophagus, 13.right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 39. aortadescendens, 46. bronchus principalis dexter, 47. bronchus principalissinister, 67. vertebra thoracica IX, 69. liver, 86. A. pulmonalis dextra,88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalissinistra.

Fig. 19. 7. esophagus, 13. right lung lobe, 17. left lung lobe, 30. tho-racic retia mirabilia, 39. aorta descendens, 46. bronchus principalisdexter, 47. bronchus principalis sinister, 69. liver, 70. vertebra thora-cica X, 86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pul-monalis dextra, 90. V. pulmonalis sinistra.

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Defense, the MMP’s animal care and use program is rou-tinely reviewed by an Institutional Animal Care and UseCommittee and the Department of Defense Bureau ofMedicine.

RESULTS

Diagnostic, high quality images were obtained in allcases. Respiratory motion was largely insignificant due

Fig. 20. 7. esophagus, 13. right lung lobe, 17. left lung lobe, 22. M.iliocostalis thoracis, 39. aorta descendens, 46. bronchus principalisdexter, 47. bronchus principalis sinister, 69. liver, 71. extremitas cau-dalis, vertebra thoracica X, 89. V. pulmonalis dextra, 90. V. pulmonalissinistra.

Fig. 21. 7. esophagus, 13. right lung lobe, 17. left lung lobe, 39. aortadescendens, 46. bronchus principalis dexter, 47. bronchus principalissinister, 69. liver, 72. vertebra thoracica XI, 90. V. pulmonalis sinistra.

Fig. 22. 7. esophagus, 13. right lung lobe, 17. left lung lobe, 22. M.iliocostalis thoracis, 39. aorta descendens, 46. bronchus principalisdexter, 47. bronchus principalis sinister, 49. articulatio capitis costae,69. liver, 73. extremitas caudalis, vertebra thoracica XI, 74. M. hypaxa-lis lumborum, 75. region of fundic chamber, 76. M. rectus abdominis.

Fig. 23. 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalis lum-borum, 39. aorta, 69. liver, 74. M. hypaxalis lumborum, 76. M. rectusabdominis, 77. gas in forestomach, 78. gas in fundic chamber, 79. ver-tebra thoracica XII.

BOTTLENOSE DOLPHIN THORACIC CT ANATOMY 909

to the species’ normal apneustic respiratory pattern, thespeed and timing of image acquisition, and the adminis-tration of mild sedation. No clinical complications wereseen in any animal during or following transport. A lat-

eral scout (Fig. 2) and contiguous corresponding trans-verse images of Animal 1 (a 27-year-old male) arepresented in cranial to caudal sequence (Figs. 3–25). Aside-by-side video of these images in soft tissue (350/40),bone (1500/300), and lung (1400/2500) window width/window level (Hounsfield units, or HU) are included asa supplemental online file.

All dolphins evaluated had 12 thoracic vertebrae. Thefirst four ribs in these animals articulated ventrallywith the flat, broad sternum and all 12 ribs articulatedwith the vertebral column. The most cranial vertebralribs in T. truncatus are double-headed (Rommel, 1990;Rommel and Lowenstine, 2001), and the capitulum andtuberculum of these ribs articulate with juxtaposed ver-tebrae. In this study, the number of double-headed ribsvaried from 3 to 5.

All four animals had a right-sided bronchus trachealisthat originated from the trachea at the level of vertebraethoracicae I and II (Fig. 8). The origin of the bronchustrachealis was on average 5.1 cm cranial to the bifurca-tio tracheae (Table 2). The average maximum diameter

Fig. 24. 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalislumborum, 39. aorta abdominalis, 74. M. hypaxalis lumborum, 77. gasin forestomach, 80. discus intervertebralis, vertebrae thoracicae XIIand XIII.

Fig. 25. 4. subdermal connective tissue sheath, 13. right lung lobe,22. M. iliocostalis lumborum, 39. aorta abdominalis, 74. M. hypaxalislumborum, 77. gas in forestomach, 81. vertebra thoracica XIII, 82. fluidin forestomach.

TABLE 2. Distance from origin of bronchus trachealisto bifurcatio tracheae

Animal Distance (cm)

1 5.422 4.113 5.434 5.41Mean 5.09 6 0.65

Fig. 26. 3D volume renderings depicting the trachea, bronchi, andlung margins in situ. The ribs, pectoral flippers, and gastrointestinalgas have been removed for clarity. (A) Dorsal oblique; the bottom ofthe image is the right side of the animal. (B) Dorsal oblique; the bot-tom of the image is the left side of the animal. (C) Dorsal aspect; theright side of the animal is to the right of the image. (D) Left side of theanimal.

910 IVAN�CIC ET AL.

of the bronchus trachealis was 1.53 cm. On average, thisrepresented 42.2% of the tracheal diameter at the samelevel (Table 3). The bifurcatio tracheae was locatedbetween the level of vertebra thoracica III and vertebraethoracicae IV and V discus intervertebralis (Fig. 9). Thisis similar to published reports of bifurcatio tracheaelocation in normal thoracic radiography of Northern ele-phant seal (Mirounga angustirostris) pups (Dennisonet al., 2009a).

In accordance with known descriptions of respiratoryanatomy in cetaceans (Fiebiger, 1916; Wislocki, 1929;Wislocki and Belanger, 1940; Wislocki 1942; Fanningand Harrison, 1972; Simpson and Gardner, 1972; Slijper,1979; Drabek and Kooyman, 1986), the right and leftlungs exhibited no lobation. Instead, the bronchus prin-cipalis dexter et sinister gradually tapered caudally as

they gave off successive bronchi lobares in varying direc-tions. These secondary bronchi in turn gave rise tosmaller bronchi segmentales. The only exception to thegently sloped branching of airways was the first branchof the bronchus trachealis. This airway extended intothe right cranioventral lung at an acute angle in all ani-mals. It formed a narrow U-shape at its origin where itwrapped around the dorsal wall of the V. costocervicalisdextra. The number of airway generations detectable onCT varied from 16 to 19, with a mean of 17 6 1.5. 3D vol-ume renderings depicting the trachea, bronchi, and lungcontours of the live T. truncatus in situ are presented inFig. 26.

The cranial border of the lung lobes extended as farcranially as the level of the fused atlas-axis (vertebraecervicalis I and II) in two animals, the intervertebraldisc space between the atlas-axis and vertebra cervicalisIII, or vertebra thoracis I. The caudal extent of the lungcharacterized by the costophrenic and lumbophrenicangles also varied slightly, from the level of vertebrathoracis XII to the level of vertebrae lumbaris II. Thecostophrenic angle is a radiographic term denoting theintersection of the ribs and the diaphragm; the lumbo-phrenic angle indicates the intersection of the columnavertebralis and the diaphragm (Blood and Studdert,1999; Muhlbauer and Kneller, 2013). These sites weredetermined from dorsal and sagittal multiplanar recon-structions of the CT data.2 As expected (Fiebiger, 1916;Wislocki, 1929; Wislocki and Belanger, 1940; Wislocki1942; Fanning and Harrison, 1972; Slijper, 1979; Drabekand Kooyman, 1986), the ventral aspect of the lung lobeswas consistently exceedingly thin where it wrappedaround the lateral margins of the heart (Figs. 12, 13).The total lung length was as follows: Animal 1 5 56.5cm, Animal 2 5 45.3 cm, Animal 3 5 54.3 cm, and Animal4 5 52.0 cm (range, 45.3–56.5 cm, mean 52.0 cm) (meas-ured as the distance between the most cranial to the

Fig. 28. 3D color volume rendering of the thorax, left lateral aspect.The near (left) ribs have been removed for clarity.

Fig. 27. 3D color volume rendering of the lung surface of Tursiopstruncatus, dorsal aspect. Cranial is at the top of the image. The rightside of the animal is to the right of the image. The bronchus trachealisis faintly seen cranial to the bifurcatio tracheae. Rib indentations arevisible on the surface of the lung parenchyma.

TABLE 3. Maximum diameter of bronchus trachealis (BT)

AnimalWeight

(kg)Length

(cm)BT diameter

(cm)

Tracheal diam.at max diam.

of BT (cm)

BT diameter aspercentage of

tracheal diameter

1 218 264 1.50 3.56 42.2%2 175 248 1.65 3.98 41.5%3 154 244 1.33 3.39 39.2%4 163 247 1.65 3.60 45.8%Mean 178 6 27.4 251 6 9.0 1.53 6 0.15 3.63 6 0.22 42.2 6 2.74%

BOTTLENOSE DOLPHIN THORACIC CT ANATOMY 911

most caudal transverse CT images that included aeratedlung tissue). A 3D volume rendering of the dorsal lungsurface of T. truncatus is presented in Fig. 27, and a360-degree angle rotating video of this 3D rendering isincluded as a supplemental online file.

In this study, the right-to-left dimension of the invivo T. truncatus heart was notably larger than thedorsal-to-ventral dimension. Average cardiac heightwas nearly half its width (Table 4), which coincidedwith the reduced thoracic height on midline relative tothe abaxial thorax (Fig. 12). A degree of thoracic col-lapse inherent in gravity loading is likely a contributingfactor to this finding. The heart occupied approximately28% of the maximum thoracic length, 54% of the maxi-mum thoracic width, and 58% of the maximum thoracicheight on midline (Table 5). The cardiac width as a per-centage of thoracic width was slightly smaller in T.truncatus compared to a width of 59%–66% in youngphocids and otariids (Dennison et al., 2009a). Maximalcardiac and thoracic dimensions were quantified usingdorsal and sagittal multiplanar reconstructions of theCT data.2

Space-occupying triangular-shaped bilaterally sym-metrical tissue ventral to the columna vertebralis anddorsal to the lungs was anatomically consistent with thethoracic and basal cranial retia mirabilia (Figs. 4–18).This hypoattenuating vascular tissue had a mean quan-titative value of �20–30 HU (Hounsfield units). It couldnot be characterized further as iodinated intravenouscontrast would be needed to delineate vascular struc-tures from surrounding soft tissue and it was not admin-istered in this pilot study.

The Lnn. cervicales superficiales located cranial to thescapulae were apparent in every animal and had quanti-fiable dimensions (Table 6; Fig. 3). The borders of theLnn. marginales were inconspicuous (Cowen and Smith,1999), however no space-occupying structures were seenat the intersection of the ventral lung and diaphragm(Fig. 17). Lnn. tracheobronchales (hilar) and Lnn. dia-phragmatis could not be identified in any animal, unlikereports of normal lymph nodes in canine thoracic CT (DeRyke et al., 2005).

DISCUSSION

The lack of conspicuity of Lnn. tracheobronchales anddiaphragmatis in this study, previously described in theT. truncatus thorax (Cowan and Smith, 1999), may bedue to lack of intravenous iodinated contrast administra-tion, may imply the structures are too small to be seenin healthy animals, or some combination of both factors.In addition, although the airways in cetaceans are rein-forced with cartilage to the level of the alveoli (Rommel

TABLE 4. Maximal cardiac dimensions

Animal Length (cm) Width (cm) Height (cm)

1 16.11 18.41 9.662 14.54 19.51 9.583 14.69 17.72 9.604 13.16 18.42 9.28Mean 14.63 6 1.22 18.52 6 0.74 9.53 6 0.17

Note that the measurements represented here are inher-ently affected by gravity-loading during out-of-water imageacquisition.

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912 IVAN�CIC ET AL.

et al., 2006) and quantification of pulmonary attenuationby measuring HU in a region of interest may revealhigher values in Tursiops relative to domestic animals,this measurement has limited clinical applicability andwas not evaluated here.

A few limitations in our study are worth noting. Thecorrelation of CT images to sections of gross anatomywith anatomic and histopathologic analysis of tissues toconfirm normalcy is ideal but could not be undertaken inthe course of clinical evaluation of healthy dolphin sub-jects. Another limitation is the relatively small number ofanimals included in the analysis. Further studies areneeded to corroborate the findings reported. The effect ofgravitational loading on the qualitative appearance andquantitative assessment of the CT images is critical toconsider, albeit unavoidable. As such, descriptions andimages in this text must be interpreted with an assump-tion of some thoracic collapse. The atlas is not intendedto be an accurate representation of the natural, fullyexpanded thorax of a T. truncatus in water, but rather toserve as a reference for antemortem on-land CT examina-tions. Finally, future acquisition of thoracic CT imagesfollowing intravenous administration of iodinated con-trast will be of enormous value in generating meaningful3D data of the vasculature in vivo and in determiningnormal enhancement patterns of thoracic soft tissues.

As medical management of marine mammals such as T.truncatus continues to improve, and access to advancedimaging increases, there will be a growing need for guid-ance on acquisition and interpretation of resultant data.This pertains not only to dolphins permanently housed inaquatic facilities but also wild dolphins temporarilyhoused in rehabilitation facilities and fresh-dead speci-mens that have washed ashore and require post-mortemevaluation. A multitude of references in the literaturedescribe both normal (Smallwood, 1982; Ahlberg et al.,1985; Zook et al., 1989; Smallwood and George, 1992;Smallwood and George, 1993; Samii et al., 1998) andabnormal (Punto et al., 1984; Spann et al., 1998; Yoonet al., 2004; Schultz and Zwingenberger, 2008; Seileret al., 2008; Joly et al., 2009; Ballegeer et al., 2010; Denn-ler et al., 2011; Marolf et al., 2011; Reetz et al., 2012; Scri-vani et al., 2012) computed tomography of the thorax interrestrial companion animals. The unique anatomicaland physiological characteristics of dolphins, however,necessitate species-specific understanding. This pilotstudy represents first detailed look at thoracic CT in a livemarine mammal. The images and illustrations in this textare meant to serve as a guide for image acquisition, a ref-erence for cross-sectional anatomy, and a manual for clini-cal interpretation of thoracic CT in bottlenose dolphins.

ACKNOWLEDGMENTS

The authors would like to thank Veronica Cendejas forher technical expertise and outstanding dedication increating the line drawings used in this text and Dr. SamH. Ridgway for his detailed review of the manuscript.We would also like to thank the Office of Naval Researchfor funding support (grant no: N0001412WX20890), theveterinary, biotechnical, and training staff of the NavyMarine Mammal Program, Peter Agbulos for his techni-cal assistance with CT image acquisition, and the NavalMedical Center San Diego.

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Width (cm) Height (cm) Width (cm) Height (cm)

1 1.51 4.33 1.13 4.342 1.94 3.86 2.10 3.893 1.58 3.41 1.77 4.104 2.10 3.49 1.66 2.95Mean 1.79 6 0.28 3.77 6 0.42 1.67 6 0.40 3.82 6 0.28

Mean SCLN width (cm) 1.74 6 0.33Mean SCLN height (cm) 3.80 6 0.49

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