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THE ANATOMICAL RECORD 297:901–915 (2014)

Computed Tomography and Cross-Sectional Anatomy of the Thorax of the Live Bottlenose Dolphin (Tursiops truncatus) ´ ,1* MAURICIO SOLANO,2 AND CYNTHIA R. SMITH1 MARINA IVANCIC 1 National Marine Mammal Foundation, San Diego, California 2 Cummings School of Veterinary Medicine, Tufts University, North Grafton, Massachusetts

ABSTRACT Pulmonary disease is one of the leading causes of cetacean morbidity and mortality in the wild and in managed collections. The purpose of this study was to present the computed tomographic (CT) appearance of the thorax of the live bottlenose dolphin (Tursiops truncatus) out-of-water and to describe the technical and logistical parameters involved in CT image acquisition in this species. Six thoracic CT evaluations of four conscious adult bottlenose dolphins were performed between April 2007 and May 2012. Animals were trained to slide out of the water onto foam pads and were transported in covered trucks to a human CT facility. Under light sedation, animals were secured in sternal recumbency for acquisition of CT data. Non-contrast helical images were obtained during an end-inspiratory breath hold. Diagnostic, high quality images were obtained in all cases. Respiratory motion was largely insignificant due to the species’ apneustic respiratory pattern. CT findings characteristic of this species include the presence of a bronchus trachealis, absence of lung lobation, cranial cervical extension of the lung, lack of conspicuity of intrathoracic lymph nodes, and presence of retia mirabilia. Dorsoventral narrowing of the heart relative to the thorax was seen in all animals and is suspected to be an artifact of gravity loading. Diagnostic thoracic computed tomography of live cetaceans is feasible and likely to prove clinically valuable. A detailed series of cross-sectional reference images is C 2014 Wiley Periodicals, Inc. provided. Anat Rec, 297:901–915, 2014. V

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

Pulmonary disease is one of the leading causes of cetacean morbidity and mortality in the wild and in managed 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 veterinarians charged with the medical care of dolphins, prompt detection of pulmonary abnormalities is imperative. This is particularly true given that underlying pulmonary disease can be clinically silent, and dolphins are adept at masking illness (McBain, 2001). Diagnostic imaging of the lungs of larger aquatic species using radiography and ultrasonography has been C 2014 WILEY PERIODICALS, INC. V

Grant sponsor: Office of Naval Research; Grant number: N0001412WX20890; Grant sponsor: Navy Marine Mammal Program. *Correspondence to: Marina Ivancˇic´; National Marine Mammal Foundation, 2240 Shelter Island Drive, Suite 200, San Diego, CA 92106. E-mail: [email protected] Received 31 March 2013; Accepted 7 January 2014. DOI 10.1002/ar.22900 Published online 4 March 2014 in Wiley Online Library (wileyonlinelibrary.com).

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902 TABLE 1. List of anatomical structures 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36. 37. 38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 48. 49. 50. 51. 52. 53. 54. 55. 56. 57. 58. 59. 60. 61. 62. 63. 64. 65. 66. 67. 68.

Trachea Articulatio atlanto-occipitalis Lnn. cervicales superficiales Subdermal connective tissue sheath M. semispinalis M. longissimus Esophagus Basal cranial retia or cervical arterial retia Mm. multifidi Vertebral body of fused atlas-axis (vertebrae cervicales I and II) Right scapula Left scapula Right lung lobe Extremitas caudalis, vertebra cervicalis III Lamina arcus, vertebra cervicalis IV M. longus capitis Left lung lobe A. subclavia sinistra Vertebra cervicalis VII Right humerus Extremitas caudalis, vertebra thoracica I M. iliocostalis A. costocervicalis dextra V. brachiocephalica sinistra Truncus brachiocephalicus dexter Bronchus trachealis V. costocervicalis dextra Left humerus Extremitas cranialis, vertebra thoracica III Thoracic retia mirabilia Vena cava cranialis Sternum Costa asternalis sinistra III M. sternocephalicus Right radius Right ulna Vertebra thoracica IV Bifurcatio tracheae Aorta Arcus aortae Bronchus lobares of the bronchus trachealis Extremitas caudalis, vertebra thoracica IV Left radius Left ulna Bronchus segmentales of bronchus principalis sinister Bronchus principalis dexter (BPD) Bronchus principalis sinister (BPS) Processus articularis cranialis, vertebra thoracica V Articulatio capitis costae Junction, costa asternalis and costa sternalis Bronchus segmentales, BPS Vertebra thoracica V Atrium dextrum Vertebra thoracica VI Bronchus lobares of BPD Bronchus segmentales of BPD Bronchus segmentales of BPS Extremitas caudalis, vertebra thoracica VI Processus spinosus, vertebra thoracica VI Ventriculus dexter Vertebra thoracica VII Vena cava caudalis Extremitas cranialis, vertebra thoracica VIII Region of Lnn. marginales Vertebra thoracica VIII Bronchus segmentales of bronchus trachealis Vertebra thoracica IX Processus spinosus, vertebra thoracica VIII

TABLE 1. (continued) 69. 70. 71. 72. 73. 74. 75. 76. 77. 78. 79. 80. 81. 82. 83. 84. 85. 86. 87. 88. 89. 90.

Liver Vertebra thoracica X Extremitas caudalis, vertebra thoracica X Vertebra thoracica XI Extremitas caudalis, vertebra thoracica XI M. hypaxalis lumborum Region of fundic chamber M. rectus abdominis Gas in forestomach Gas in fundic chamber Vertebra thoracica XII Discus intervertebralis, vertebrae thoracicae XII and XIII Vertebra thoracica XIII Fluid in forestomach Bronchus lobares, BPS M. sternohyoideus Heart A. pulmonalis dextra Costa sternalis A. pulmonalis sinistra V. pulmonalis dextra V. pulmonalis sinistra

reported (Van Bonn et al., 2001; Smith et al., 2012). These thoracic imaging techniques have inherent limitations and challenges. With radiography, the entirety of the lung cannot be evaluated in a single image. Eight to ten sectional radiographs are commonly needed to evaluate the thorax in bottlenose dolphins, where the animal can weigh more than 300 kg (Van Bonn et al., 2001). In addition, large patient size necessitates higher exposure settings. Generators capable of producing X-rays powerful enough to penetrate large animal patients are not typically hand-held, and therefore not readily available in the field (Pease, 2009). Further, radiography of the thorax requires a dolphin to be removed from the water. Thoracic ultrasonography can be performed with the dolphin either in or out of the water, however only the periphery of the thorax can be evaluated due to acoustic shadowing from air-filled lung. Examination has proven to be clinically valuable but is limited to the thoracic wall, intercostal muscles, pleural surface, and peripheral lymph nodes in healthy animals (Smith et al., 2012). Deeper structures can be seen but require the presence of peripheral lung consolidation or a mild to moderate volume of pleural effusion (Rantanen, 1986; Reef et al., 1991; Tidwell, 1998; Reichle and Wisner, 2000). Acoustic shadowing deep to each rib also limits evaluation. The depth of penetration of an ultrasound transducer is limited by its wavelength, and wavelength is inversely proportional to frequency. The frequency of the transducer also dictates the axial spatial resolution of the image (along the axis of the beam). Hence, in order to penetrate deeper tissues in larger animals, transducers that use longer wavelengths and lower frequencies are needed. This results in decreased spatial resolution (Rantanen, 1986; Reef et al., 1991). Computed tomography (CT) is a cross-sectional diagnostic imaging modality that allows detailed examination of the entire thorax. This modality is not susceptible to the intrinsic superimposition limitations of radiography (Prather et al., 2005), or the acoustic shadowing and depth limitations of ultrasonography.

BOTTLENOSE DOLPHIN THORACIC CT ANATOMY

Current CT technology can generate detailed thoracic images with high tissue contrast resolution and only slightly decreased spatial resolution relative to digital radiography. As multi-detector (multi-slice) CT scanners are becoming increasingly available (Habing et al., 2010; Drees et al., 2011), rapid assessment of large anatomical regions is possible. This is of particular value in cetaceans, since sizeable volumes of tissue must be evaluated while minimizing time on land. A number of

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

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previous investigations have described cross-sectional diagnostic imaging in marine mammals, most recently of the thorax (Alonso-Farre et al., 2013), however with few exceptions (Finneran, 2003; Dennison et al., 2009b; Montie et al., 2011) nearly all of these studies have been performed post-mortem (Marino et al., 2001a, b, c, 2002, 2003a, b, c, 2004a, b; Liste et al., 2006; Dennison and Schwarz, 2008; Ketten and Montie, 2008; Moore et al., 2009; Moore et al., 2011; Dennison et al., 2012; AlonsoFarre et al., 2013). Despite their important scientific value, their clinical applicability is limited.

Fig. 3. Figures 3–25 include (A) a line drawing detailing anatomical structures, 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 all images. Figure number corresponds to the reference line number in Fig. 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

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

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Fig. 4. 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, 10. vertebral body of fused atlas-axis (vertebrae cervicales I and II), 11. right scapula, 12. left scapula, 13. cupula of right lung lobe, 84. M. sternohyoideus.

Fig. 6. 1. trachea, 4. subdermal connective tissue sheath, 7. esophagus, 8. basal cranial retia or cervical arterial retia, 9. Mm. multifidi, 11. right scapula, 12. left scapula, 13. right lung lobe, 16. M. longus capitis, 17. cupula of left lung lobe, 18. A. subclavia sinistra, 19. vertebra cervicalis VII, 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. right scapula, 12. left scapula, 13. cupula of right lung lobe, 14. extremitas caudalis, vertebra cervicalis III, 15. lamina arcus, vertebra cervicalis IV, 16. M. longus colli, 84. M. sternohyoideus.

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

The Navy Marine Mammal Program (MMP) first began 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 monitoring pulmonary parenchymal abnormalities. The purpose


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. right humerus, 23. A. costocervicalis dextra, 25. truncus brachiocephalicus dexter, 26. bronchus trachealis, 27. V. costocervicalis dextra, 28. caput humerus sinister, 29. extremitas cranialis, vertebra thoracica III, 30. thoracic retia mirabilia, 31. vena cava cranialis, 32. sternum, 33. costa asternalis sinistra III.

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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. right radius, 36. right ulna, 39. aorta descendens, 42. extremitas caudalis, vertebra thoracica IV, 43. left radius, 44. left ulna, 45. bronchus segmentales of bronchus principalis sinister, 46. bronchus principalis dexter, 47. bronchus principalis sinister, 48. processus articularis cranialis, vertebra thoracica V, 49. articulatio capitis costae, 50. junction, costa asternalis and costa sternalis, 66. bronchus segmentales of bronchus trachealis, 85. heart. Note the asymmetrical appearance of the thorax in 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 pectoral flipper and the left-sided ribs have a more angular appearance, consistent with some out-of-water thoracic collapse.

of this study is to present the CT appearance of the thorax of the conscious, healthy bottlenose dolphin (Tursiops truncatus) and to describe the logistics involved in CT image acquisition for this aquatic species. To our knowledge, this is the first detailed anatomical report of extra-cranial cross-sectional diagnostic imaging of a live marine mammal species.

MATERIALS AND METHODS

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

Thoracic computed tomographic evaluations of four healthy live adult bottlenose dolphins were performed between April 2007 and May 2012. This included three males and one female (age range, 11–28 years, mean 16.8 years; weight range, 154–218 kg, mean 177 kg; length range, 244–264 cm, mean 251 cm). One animal was evaluated on three separate occasions. All other animals were evaluated once. At the time of each evaluation, individual animal measurements were as follows: Animal 1 5 264 cm total body length, 213–218 kg total body weight (varied across three scans); Animal 2 5 248 cm total body length, 175 kg total body weight; Animal 3 5 244 cm total body length, 154 kg total body weight; Animal 4 5 247 cm total body length, 163 kg total body weight (total body length here is defined as the distance from the tip of the rostrum to the caudal margin of the

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Fig. 11. 4. subdermal connective tissue sheath, 7. esophagus, 13. right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 32. sternum, 34. M. sternocephalicus, 43. left radius, 44. left ulna, 46. bronchus principalis dexter, 47. bronchus principalis sinister (BPS), 51. bronchus segmentales, BPS, 52. vertebra thoracica V, 53. atrium dextrum, 85. Heart. Note the asymmetrical appearance of the thorax in 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 pectoral flipper and the left-sided ribs have a more angular appearance, consistent with some out-of-water thoracic collapse.

tail flukes on midline). None of the animals had clinical evidence of thoracic disease or hematological or biochemical evidence of infection or inflammation. The dolphins were removed from open ocean pens at the MMP either by voluntarily beaching onto foam pads or by swimming into stretchers. One animal was premedicated with oral diazepam 0.13 mg/kg prior to beaching. The animals were transported 8.5 miles in covered trucks to a human medical facility. Veterinary personnel continuously monitored basic physiological parameters including heart rate, respiratory rate, and ECG (electrocardiography). Light sedation was administered on arrival (0.02–0.09 mg/kg intramuscular midazolam in the M. longissimus dorsi lateral to the dorsal fin). CT equipment was protected with plastic sheeting. The animals were secured in sternal recumbency with tucked pectoral flippers and transferred to the CT table using a human spine board (Fig. 1). Water was intermittently and judiciously misted onto the animals’ skin. Care was taken in positioning the dolphins as upright as possible to minimize atelectasis, undue pressure on the pectoral flippers, and image obliquity/asymmetry. CT evaluation of the thorax was performed by scanning from the occiput to the mid-level of the dorsal fin in conjunction with other regions of clinical interest specific to each animal’s medical history (head, ears, kidneys, and/or humeral joints). Images were acquired using a multi-detector 16-slice helical CT scanner with an 80 cm bore and 227 kg table

Fig. 12. 4. subdermal connective tissue sheath, 5. M. semispinalis thoracis, 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 principalis dexter (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.

weight limit.1 Non-contrast CT images were obtained opportunistically during an end-inspiratory breath-hold characteristic of cetaceans. Image acquisition was initiated immediately following inhalation, and the entire region of interest was scanned during a single breathhold. Technical parameters included a standard algorithm, 140 kVp (kilovolt potential) to minimize beam hardening, automatically generated mA (milliamperes) (range, 300–715), a rotational speed of 0.5 sec, and a pitch of 1.75 to minimize scan time. Helical 1.25 mm slices with data interpolation were obtained initially and retrospectively reconstructed to overlapping 1.25 mm 3 0.625 mm series in soft tissue, lung, and bone reconstruction algorithms. The dolphins were immediately transported back to ocean enclosures following the scan. A reversal agent was administered (0.003–0.012 mg/kg flumazenil) either intravenously in the caudal peduncle periarterial venous rete, the ventral fluke periarterial venous rete, or intramuscularly in the M. longissimus dorsi following three of the six CT scans. This was given after departure from the human medical facility and prior to water re-entry. The average CT scan time was 50 min and the average duration of time out of the water was 3 hr. All thoracic CT studies were evaluated at the time of image acquisition for clinical purposes by the attending veterinarian and retrospectively by a board-certified veterinary radiologist (MI) for the purpose of this publication. Dedicated open-source DICOM (digital imaging 1

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


Fig. 13. 4. subdermal connective tissue sheath, 7. esophagus, 9. Mm. multifidi, 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalis thoracis, 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 spinosus, 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. sternum, 39. aorta descendens, 46. bronchus principalis dexter, 47. bronchus principalis sinister, 61. vertebra thoracica VII, 62. vena cava caudalis, 85. heart, 86. A. pulmonalis dextra, 87. costa sternalis, 88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

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Fig. 15. 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. bronchus principalis sinister, 62. vena cava caudalis, 63. extremitas cranialis, vertebra thoracica VIII, 85. heart, 86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

communications in medicine) viewing software2 was used for qualitative and quantitative image analysis. Line drawings were created by hand-tracing each CT image with a computer mouse using commercially available illustration software.3 The line drawings were utilized to detail relevant anatomy without compromising the quality of the CT images (Figs. 3–25). Anatomical references used include 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 and Kamiya, 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 and Lowenstine, 2001; Buchholtz and Schur, 2004; De Ryke et al., 2005; World Association of Veterinary Anatomists, 2005; Rommel et al., 2006, 2007; Cooper et al., 2007; Cotten et al., 2008; Piscitelli et al., 2010; Costidis and Rommel, 2012). Mean values and standard deviations for anatomical measurements were calculated using an online open-source statistics calculator.4 The MMP is accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International and adheres to the national standards of the United States Public Health Service Policy on the Humane Care and Use of Laboratory Animals and the Animal Welfare Act. As required by the Department of 2

Osirix 4.0, Pixmeo, Geneva, Switzerland Adobe Illustrator CS6, Adobe Systems, San Jose, California Standard Deviation Calculator. Web. 28 Feb, 2013. http://easycalculation.com/statistics/standard-deviation.php 3 4

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Fig. 16. 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. bronchus principalis sinister (BPS), 49. articulatio capitis costae, 64. region of Lnn. marginales, 65. vertebra thoracica VIII, 83. bronchus lobares, BPS, 85. heart, 86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 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. bronchus principalis sinister, 67. vertebra thoracica IX, 68. processus spinosus, vertebra thoracica VIII, 69. liver, 86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

Fig. 18. 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. bronchus principalis sinister, 67. vertebra thoracica IX, 69. liver, 86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

Fig. 19. 7. esophagus, 13. right lung lobe, 17. left lung lobe, 30. thoracic retia mirabilia, 39. aorta descendens, 46. bronchus principalis dexter, 47. bronchus principalis sinister, 69. liver, 70. vertebra thoracica X, 86. A. pulmonalis dextra, 88. A. pulmonalis sinistra, 89. V. pulmonalis dextra, 90. V. pulmonalis sinistra.

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Fig. 20. 7. esophagus, 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalis thoracis, 39. aorta descendens, 46. bronchus principalis dexter, 47. bronchus principalis sinister, 69. liver, 71. extremitas caudalis, vertebra thoracica X, 89. V. pulmonalis dextra, 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 principalis dexter, 47. bronchus principalis sinister, 49. articulatio capitis costae, 69. liver, 73. extremitas caudalis, vertebra thoracica XI, 74. M. hypaxalis lumborum, 75. region of fundic chamber, 76. M. rectus abdominis.

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

Fig. 23. 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalis lumborum, 39. aorta, 69. liver, 74. M. hypaxalis lumborum, 76. M. rectus abdominis, 77. gas in forestomach, 78. gas in fundic chamber, 79. vertebra thoracica XII.

Defense, the MMP’s animal care and use program is routinely reviewed by an Institutional Animal Care and Use Committee and the Department of Defense Bureau of Medicine.

RESULTS Diagnostic, high quality images were obtained in all cases. Respiratory motion was largely insignificant due

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Fig. 24. 13. right lung lobe, 17. left lung lobe, 22. M. iliocostalis lumborum, 39. aorta abdominalis, 74. M. hypaxalis lumborum, 77. gas in forestomach, 80. discus intervertebralis, vertebrae thoracicae XII and XIII.

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

TABLE 2. Distance from origin of bronchus trachealis to bifurcatio tracheae Animal 1 2 3 4 Mean

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

to the species’ normal apneustic respiratory pattern, the speed and timing of image acquisition, and the administration of mild sedation. No clinical complications were seen in any animal during or following transport. A lat-

Distance (cm) 5.42 4.11 5.43 5.41 5.09 6 0.65

eral scout (Fig. 2) and contiguous corresponding transverse images of Animal 1 (a 27-year-old male) are presented in cranial to caudal sequence (Figs. 3–25). A side-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 as a supplemental online file. All dolphins evaluated had 12 thoracic vertebrae. The first four ribs in these animals articulated ventrally with the flat, broad sternum and all 12 ribs articulated with the vertebral column. The most cranial vertebral ribs in T. truncatus are double-headed (Rommel, 1990; Rommel and Lowenstine, 2001), and the capitulum and tuberculum of these ribs articulate with juxtaposed vertebrae. In this study, the number of double-headed ribs varied from 3 to 5. All four animals had a right-sided bronchus trachealis that originated from the trachea at the level of vertebrae thoracicae I and II (Fig. 8). The origin of the bronchus trachealis was on average 5.1 cm cranial to the bifurcatio tracheae (Table 2). The average maximum diameter


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TABLE 3. Maximum diameter of bronchus trachealis (BT)

Animal 1 2 3 4 Mean

Weight (kg)

Length (cm)

BT diameter (cm)

Tracheal diam. at max diam. of BT (cm)

BT diameter as percentage of tracheal diameter

218 175 154 163 178 6 27.4

264 248 244 247 251 6 9.0

1.50 1.65 1.33 1.65 1.53 6 0.15

3.56 3.98 3.39 3.60 3.63 6 0.22

42.2% 41.5% 39.2% 45.8% 42.2 6 2.74%

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 Tursiops truncatus, dorsal aspect. Cranial is at the top of the image. The right side of the animal is to the right of the image. The bronchus trachealis is faintly seen cranial to the bifurcatio tracheae. Rib indentations are visible on the surface of the lung parenchyma.

of the bronchus trachealis was 1.53 cm. On average, this represented 42.2% of the tracheal diameter at the same level (Table 3). The bifurcatio tracheae was located between the level of vertebra thoracica III and vertebrae thoracicae IV and V discus intervertebralis (Fig. 9). This is similar to published reports of bifurcatio tracheae location in normal thoracic radiography of Northern elephant seal (Mirounga angustirostris) pups (Dennison et al., 2009a). In accordance with known descriptions of respiratory anatomy in cetaceans (Fiebiger, 1916; Wislocki, 1929; Wislocki and Belanger, 1940; Wislocki 1942; Fanning and Harrison, 1972; Simpson and Gardner, 1972; Slijper, 1979; Drabek and Kooyman, 1986), the right and left lungs exhibited no lobation. Instead, the bronchus principalis dexter et sinister gradually tapered caudally as

they gave off successive bronchi lobares in varying directions. These secondary bronchi in turn gave rise to smaller bronchi segmentales. The only exception to the gently sloped branching of airways was the first branch of the bronchus trachealis. This airway extended into the right cranioventral lung at an acute angle in all animals. It formed a narrow U-shape at its origin where it wrapped around the dorsal wall of the V. costocervicalis dextra. The number of airway generations detectable on CT varied from 16 to 19, with a mean of 17 6 1.5. 3D volume renderings depicting the trachea, bronchi, and lung contours of the live T. truncatus in situ are presented in Fig. 26. The cranial border of the lung lobes extended as far cranially as the level of the fused atlas-axis (vertebrae cervicalis I and II) in two animals, the intervertebral disc space between the atlas-axis and vertebra cervicalis III, or vertebra thoracis I. The caudal extent of the lung characterized by the costophrenic and lumbophrenic angles also varied slightly, from the level of vertebra thoracis XII to the level of vertebrae lumbaris II. The costophrenic angle is a radiographic term denoting the intersection of the ribs and the diaphragm; the lumbophrenic angle indicates the intersection of the columna vertebralis and the diaphragm (Blood and Studdert, 1999; Muhlbauer and Kneller, 2013). These sites were determined from dorsal and sagittal multiplanar reconstructions of the CT data.2 As expected (Fiebiger, 1916; Wislocki, 1929; Wislocki and Belanger, 1940; Wislocki 1942; Fanning and Harrison, 1972; Slijper, 1979; Drabek and Kooyman, 1986), the ventral aspect of the lung lobes was consistently exceedingly thin where it wrapped around the lateral margins of the heart (Figs. 12, 13). The total lung length was as follows: Animal 1 5 56.5 cm, Animal 2 5 45.3 cm, Animal 3 5 54.3 cm, and Animal 4 5 52.0 cm (range, 45.3–56.5 cm, mean 52.0 cm) (measured as the distance between the most cranial to the

58.4% 59.5% 61.6% 51.3% 57.7 6 4.47 16.54 16.09 15.59 18.08 16.58 6 1.08 9.66 9.58 9.60 9.28 9.53 6 0.17 27.4% 32.0% 28.0% 25.0% 28.1 6 2.91% 58.7 45.5 52.5 52.8 52.4 6 5.4 16.1 14.5 14.7 13.2 14.6 6 1.2 52.6% 59.0% 51.8% 53.0% 54.1 6 3.3%

Note that the measurements represented here are inherently affected by gravity-loading during out-of-water image acquisition.

The lack of conspicuity of Lnn. tracheobronchales and diaphragmatis in this study, previously described in the T. truncatus thorax (Cowan and Smith, 1999), may be due to lack of intravenous iodinated contrast administration, may imply the structures are too small to be seen in healthy animals, or some combination of both factors. In addition, although the airways in cetaceans are reinforced with cartilage to the level of the alveoli (Rommel

18.4 19.5 17.7 18.4 18.5 6 0.7

DISCUSSION

1 2 3 4 Mean

most caudal transverse CT images that included aerated lung tissue). A 3D volume rendering of the dorsal lung surface of T. truncatus is presented in Fig. 27, and a 360-degree angle rotating video of this 3D rendering is included as a supplemental online file. In this study, the right-to-left dimension of the in vivo T. truncatus heart was notably larger than the dorsal-to-ventral dimension. Average cardiac height was nearly half its width (Table 4), which coincided with the reduced thoracic height on midline relative to the abaxial thorax (Fig. 12). A degree of thoracic collapse inherent in gravity loading is likely a contributing factor to this finding. The heart occupied approximately 28% of the maximum thoracic length, 54% of the maximum thoracic width, and 58% of the maximum thoracic height on midline (Table 5). The cardiac width as a percentage of thoracic width was slightly smaller in T. truncatus compared to a width of 59%–66% in young phocids and otariids (Dennison et al., 2009a). Maximal cardiac and thoracic dimensions were quantified using dorsal and sagittal multiplanar reconstructions of the CT data.2 Space-occupying triangular-shaped bilaterally symmetrical tissue ventral to the columna vertebralis and dorsal to the lungs was anatomically consistent with the thoracic and basal cranial retia mirabilia (Figs. 4–18). This hypoattenuating vascular tissue had a mean quantitative value of 20–30 HU (Hounsfield units). It could not be characterized further as iodinated intravenous contrast would be needed to delineate vascular structures from surrounding soft tissue and it was not administered in this pilot study. The Lnn. cervicales superficiales located cranial to the scapulae were apparent in every animal and had quantifiable dimensions (Table 6; Fig. 3). The borders of the Lnn. marginales were inconspicuous (Cowen and Smith, 1999), however no space-occupying structures were seen at the intersection of the ventral lung and diaphragm (Fig. 17). Lnn. tracheobronchales (hilar) and Lnn. diaphragmatis could not be identified in any animal, unlike reports of normal lymph nodes in canine thoracic CT (De Ryke et al., 2005).

TABLE 5. Maximum cardiac dimensions relative to the thorax

Note that the measurements represented here are inherently affected by gravity-loading during out-of-water image acquisition.

Max cardiac height (cm)

9.66 9.58 9.60 9.28 9.53 6 0.17

Max thoracic length (cm)

18.41 19.51 17.72 18.42 18.52 6 0.74

Max cardiac length (cm)

16.11 14.54 14.69 13.16 14.63 6 1.22

Max thoracic width (cm)

1 2 3 4 Mean

Max cardiac width (cm)

Height (cm)

Animal

Width (cm)

Max cardiac length as % of max thoracic length

Length (cm)

Max cardiac width as % of max thoracic width

Animal

Max thoracic height on midline (cm)

TABLE 4. Maximal cardiac dimensions

35.0 33.1 34.2 34.8 34.3 6 0.9

Max cardiac height as a % of max midline thoracic height

´ ET AL. IVANCIC

912

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TABLE 6. Dimensions of Lnn. cervicales superficiales (SCLN) Right SCLN

Left SCLN

Animal

Width (cm)

Height (cm)

Width (cm)

Height (cm)

1 2 3 4 Mean

1.51 1.94 1.58 2.10 1.79 6 0.28

4.33 3.86 3.41 3.49 3.77 6 0.42

1.13 2.10 1.77 1.66 1.67 6 0.40

4.34 3.89 4.10 2.95 3.82 6 0.28

Mean SCLN width (cm) Mean SCLN height (cm)

et al., 2006) and quantification of pulmonary attenuation by measuring HU in a region of interest may reveal higher values in Tursiops relative to domestic animals, this measurement has limited clinical applicability and was not evaluated here. A few limitations in our study are worth noting. The correlation of CT images to sections of gross anatomy with anatomic and histopathologic analysis of tissues to confirm normalcy is ideal but could not be undertaken in the course of clinical evaluation of healthy dolphin subjects. Another limitation is the relatively small number of animals included in the analysis. Further studies are needed to corroborate the findings reported. The effect of gravitational loading on the qualitative appearance and quantitative assessment of the CT images is critical to consider, albeit unavoidable. As such, descriptions and images in this text must be interpreted with an assumption of some thoracic collapse. The atlas is not intended to be an accurate representation of the natural, fully expanded thorax of a T. truncatus in water, but rather to serve as a reference for antemortem on-land CT examinations. Finally, future acquisition of thoracic CT images following intravenous administration of iodinated contrast will be of enormous value in generating meaningful 3D data of the vasculature in vivo and in determining normal enhancement patterns of thoracic soft tissues. As medical management of marine mammals such as T. truncatus continues to improve, and access to advanced imaging increases, there will be a growing need for guidance on acquisition and interpretation of resultant data. This pertains not only to dolphins permanently housed in aquatic facilities but also wild dolphins temporarily housed in rehabilitation facilities and fresh-dead specimens that have washed ashore and require post-mortem evaluation. A multitude of references in the literature describe both normal (Smallwood, 1982; Ahlberg et al., 1985; Zook et al., 1989; Smallwood and George, 1992; Smallwood and George, 1993; Samii et al., 1998) and abnormal (Punto et al., 1984; Spann et al., 1998; Yoon et al., 2004; Schultz and Zwingenberger, 2008; Seiler et al., 2008; Joly et al., 2009; Ballegeer et al., 2010; Dennler et al., 2011; Marolf et al., 2011; Reetz et al., 2012; Scrivani et al., 2012) computed tomography of the thorax in terrestrial companion animals. The unique anatomical and physiological characteristics of dolphins, however, necessitate species-specific understanding. This pilot study represents first detailed look at thoracic CT in a live marine mammal. The images and illustrations in this text are meant to serve as a guide for image acquisition, a reference for cross-sectional anatomy, and a manual for clinical interpretation of thoracic CT in bottlenose dolphins.

1.74 6 0.33 3.80 6 0.49

ACKNOWLEDGMENTS The authors would like to thank Veronica Cendejas for her technical expertise and outstanding dedication in creating the line drawings used in this text and Dr. Sam H. Ridgway for his detailed review of the manuscript. We would also like to thank the Office of Naval Research for funding support (grant no: N0001412WX20890), the veterinary, biotechnical, and training staff of the Navy Marine Mammal Program, Peter Agbulos for his technical assistance with CT image acquisition, and the Naval Medical Center San Diego.

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