THE USE OF MAGNETIC RESONANCE IMAGING TO BETTER DEFINE HOOF PATHOLOGY IN THE RETICULATED GIRAFFE (GIRAFFA CAMELOPARDALIS RETICULATA) Author(s): Kyle A. Wakeman, D.V.M., Carlos R. Sanchez, D.V.M., M.Sc., Nancy P. Lung, V.M.D., M.Sc., Jake Hersman, D.V.M., and Myra F. Barrett, D.V.M, Dipl. A.C.V.R. Source: Journal of Zoo and Wildlife Medicine, 45(3):668-671. 2014. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2013-0140R1.1 URL: http://www.bioone.org/doi/full/10.1638/2013-0140R1.1

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Journal of Zoo and Wildlife Medicine 45(3): 668–671, 2014 Copyright 2014 by American Association of Zoo Veterinarians

THE USE OF MAGNETIC RESONANCE IMAGING TO BETTER DEFINE HOOF PATHOLOGY IN THE RETICULATED GIRAFFE (GIRAFFA CAMELOPARDALIS RETICULATA) Kyle A. Wakeman, D.V.M., Carlos R. Sanchez, D.V.M., M.Sc., Nancy P. Lung, V.M.D., M.Sc., Jake Hersman, D.V.M., and Myra F. Barrett, D.V.M, Dipl. A.C.V.R.

Abstract: A 22-yr-old bull giraffe (Giraffa camelopardalis reticulata) with severely altered hoof conformation in both forelimbs was presented for necropsy following acute mortality. Due to multiple challenges that prevented safe immobilization, corrective hoof trimming procedures were never performed on this animal. To better define the extent of the damage of the soft tissue structures and bone within the hoof, a magnetic resonance imaging (MRI) system was used to obtain images of these structures. The MRI study found evidence of severe osteolysis, phalangeal fractures of both forelimbs, and tenosynovitis of several tendon sheaths. These findings help demonstrate the impact that hoof overgrowth can have on internal structures within the hoof. By managing hoof problems early in the course of disease and investing in appropriate facilities that make giraffe immobilization safer, morbidity and mortality associated with hoof disease and overgrowth can potentially be reduced. Key words: Giraffe, hoof abnormalities, hoof trimming, lameness, MRI, zoo management.

BRIEF COMMUNICATION Giraffes are characterized as artiodactylids (even-toed ungulates) based on the anatomic conformation of the hoof distal to the fetlock joint.11 As with their two-toed domestic counterparts, overgrown hooves can be a significant problem for giraffes in captivity.3,5 Due to the dangerous disposition of these animals, as well as to a unique anatomy and physiology that creates inherent risks with chemical immobilization, hoof trimming poses a significant challenge. For zoologic institutions, this makes recognizing the factors that influence hoof health and early intervention of hoof disease important considerations when managing these animals in captivity. By pursuing hoof problems early in the course of the disease, a favorable outcome is more likely to be achieved.11 This report conveys the importance of this principle by describing the magnetic resonance imaging (MRI) findings of an adult bull giraffe’s distal limbs following a 5-yr history of progressively abnormal hoof conformation. From Western University of Health Sciences, 309 East Second Street, Pomona, California 91766, USA (Wakeman); the Fort Worth Zoo, 1989 Colonial Parkway, Fort Worth, Texas 76109, USA (Sanchez, Lung); Animal Imaging, 6112 Riverside Drive, Irving, Texas, 75039, USA (Hersman); and Inside Information Radiology: a Veterinary Diagnostic Imaging Company LLC, 708 Garfield Street, Fort Collins, Colorado 80524, USA (Barrett). Correspondence should be directed to Dr. Sanchez ([email protected]).

In 2013, a 22-yr-old bull giraffe (Giraffa camelopardalis reticulata) was presented for necropsy following acute mortality unrelated to the forelimb hoof abnormalities. At the time of death this animal was being treated for a 10-yr history of progressive, bilateral forelimb lameness and stiffness, with a 5-yr history of progressive abnormal hoof overgrowth in all feet. Throughout this time period, a compounded NSAID (Ibuprofen 20 mg/ml, Diamondback Drugs, Scottsdale, Arizona 85251, USA) (3–6 g [3–6 mg/kg] p.o. s.i.d.) and a glucosamine/chondroitin supplement (GLCt 5500, GLCDirect, LLC, Paris, Kentucky 40361, USA) (13 g [13 mg/kg] p.o. s.i.d.) were used as needed to alleviate pain and support joint health. While the lameness improved, it was reoccurring and did not completely resolve. When this giraffe was found, it was laterally recumbent with signs of trauma likely caused by attempts to stand in the stall. During gross necropsy there were multifocal pale areas in the rear limb muscles suggestive of capture myopathy. The giraffe appeared in adequate body condition, with serous atrophy present in multiple fat stores. Other significant findings were well-encapsulated abscesses in the jaw and the lung containing organisms that were acid-fast negative. Histopathology results attributed death to a combination of disseminated intravascular coagulation (DIC) and confirmed rhabdomyolysis. While the underlying cause could not be definitively determined, it was thought that the DIC was mediated by sepsis, most likely associated with the Streptococcus-harboring abscesses found in the lung and jaw.

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Figure 1. Sagittal magnetic resonance image of the third digit of the right front foot of adult giraffe (G. c. reticulata) following chronic hoof over-growth. P1, phalanx 1; P2, phalanx 2; P3, phalanx 3; N, navicular bone. Black arrowheads, areas of osteolysis and degeneration; white arrowhead, osseous proliferation; large arrow, fracture of palmar process of the third phalanx with hyperextension interphalangeal joint; small arrows, areas of tenosynovitis within digital sheaths.

Examination of the hind limbs revealed only mild to moderate overgrowth of the hoof walls with no other significant pathology grossly evident. Both distal forelimbs, however, showed evidence of chronic degenerative and destructive changes. These included moderate eburnation and subchondral bone exposure on the articular surface of each phalanx. Within the distal interphalangeal joints, there was marked fibrous connective tissue present and multiple areas of mild to moderate hemorrhage. The soles of the feet did not appear to be ulcerated, and there was no gross evidence of abscesses or penetrating wounds. In this case, histopathology was not performed on the distal forelimbs. Magnetic resonance imaging (Siemens Verio 3t Tesla, Siemens Medical Solutions USA, Inc., Malvern, Pennsylvania 19355, USA) was performed on both distal forelimbs. These images were used to supplement the gross necropsy findings (Figs. 1, 2). Findings in both feet included severe, multifocal osteolysis of the distal phalanges of all digits and navicular bones of both forelimbs. Also noted were proximally displaced biaxial fractures of the palmar processes of the distal phalanges of both forelimbs. A significant

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amount of proliferative tissue was seen between the fractured portion of the distal phalanx and the body of the distal phalanx, indicating a chronic injury. There was hyperextension of both distal interphalangeal joints to the degree that a majority of load-bearing pressure was focused on the second phalanx. This was presumed to be a consequence of the chronic fractures that would have disrupted the normal function of the deep digital flexor tendon. Consequently, the distal phalanx was found tipped up in hyperextension. While there was generalized tenosynovitis of all the digital sheaths, a more-severe tendinosis was noted in the right deep digital flexor tendon of the third digit. These findings indicated that any corrective hoof trimming performed at this stage of disease would not have been curative and most likely would have had minimal effect on this animal’s progressive lameness. The severe pathology in the distal forelimbs would have resulted in continued deterioration of the giraffe’s quality of life. While this diagnostic modality is not feasible for antemortem diagnostics in a giraffe, this advanced imaging demonstrated how bone and soft tissues of the distal limbs can be altered following chronic hoof overgrowth. These findings also help demonstrate the importance of understanding the factors involved with giraffe hoof health and the positive impact of early intervention. Because the factors that influence hoof health have not been well studied in giraffes, it may be applicable to use dairy cattle as a model, given the anatomic similarities between the bovine hoof and that of most nondomestic artiodactylids. Due to the negative impact that hoof disease can have on milk productivity within dairy herds, there has been extensive research in this area.7 Laminitis, environment, nutrition, and individual genetics have all been identified as influential factors in the hoof health of dairy cattle, and it is believed that these same factors can influence hoof health of nondomestic species in a similar manner.6 While laminitis was theorized to be a cause for the initial forelimb lameness in this giraffe, it was never confirmed. At necropsy there was limited gross evidence within the hoof walls that supported past laminitis, and the forestomach was grossly and histologically unremarkable. Also, when laminitis and heel overgrowth occurs, the distal phalanx tends to be rotated downward and not hyperextended, as was the case with this animal. This, however, remains a problem in captive wild ruminants and often results from a

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Figure 2. Postmortem sagittal section of the third digit of the right front foot of adult giraffe (G. c. reticulata) showing the severe hyperextension and degenerative changes present within the distal interphalangeal joint (large black arrow). P1, phalanx 1; P2, phalanx 2; P3, phalanx 3; N, navicular bone. Small arrows, areas of osteolysis and degeneration; arrow heads, areas of hemorrhage.

dietary imbalance favoring easily digestible carbohydrates over roughage.8 In domestic cattle, regardless of the underlying cause, hooves affected by laminitis grow at increased rates and, therefore, must be regularly maintained because these growth rates will not return to normal.10 Due to the strong nutritional component of this problem, correct feeding management of ruminants in captivity is essential and has been recently reviewed for the giraffe.9 Keeping this in mind, it is important for institutions to be familiar with the impact that different dietary components can have on hoof health in captive ruminants. The role of surface substrate is another factor that could be relevant to this case. Surface environment is key to facilitating normal wear of these claws, which is important in maintenance of proper hoof conformation. While hoof pathology is common in giraffes in captivity, it has not been well documented in free-ranging animals.1 In zoos, this species tends to have finite space available to roam, increasing the dependence of hoof wear on the surface environment itself. Depending on the type and abrasiveness of the surface, the contour of the hoof can become altered, resulting in poor hoof conformation over time.10 The giraffe in this report spent the majority of time on chat, grass, and concrete. While this bull did develop severe overgrowth, this did not occur in the first 15 yr in this exhibit, nor have herd mates developed the same degree of hoof abnormalities over the same 20-yr period. There-

fore, while surface substrate is known to impact hoof health in domestic cattle, other intrinsic factors may have also contributed in this case. When hoof conformation problems arise, functional and corrective hoof trimming procedures should be performed to help restore and maintain a normal hoof conformation.12 These procedures have been outlined for dairy cattle and have also been reported for giraffes in captivity.3,5 More recently, normal hoof angles from wild giraffes have been recorded to assist with maintaining a normal hoof conformation in captive giraffes.5 However, given the inherent dangers involved with chemical immobilization, even the mostroutine procedures take careful planning, welldesigned facilities, and experienced handlers to ensure the safety of both staff and animal. The long necks, large size, and unique cardiovascular physiology of the giraffe present significant anesthetic challenges.4 In this case, the major challenges preventing corrective hoof trimming included not having the animal conditioned for restraint and the lack of appropriate facilities for safe chemical immobilization. These challenges exist at numerous zoos that house giraffes. For this reason it is essential for institutions to be proactive about performing routine hoof care under positive reinforcement or to invest in proper restraint devices to facilitate chemical immobilization.2 By performing hoof trimming early in the course of overgrowth, the need for recumbent chemical immobilization can be avoided or reduced in frequency. Operant conditioning, combined with well-designed restraint devices, will allow for excellent hoof care and long-term hoof health.2 Hoof overgrowth alters hoof conformation in such a way that the weight-bearing pressure is shifted.10 If hoof overgrowth is not addressed, this shift in load-bearing can cause injuries to soft tissue structures, phalangeal fractures, and the development of degenerative arthritis. The magnetic resonance images from this bull giraffe’s distal limbs demonstrate the long-term impact of these changes on supporting structures within the hoof. In this case, the degenerative and pathologic changes present in the distal digits would have made any corrective hoof trimming at this point unsuccessful, demonstrating the importance of proactive management of hoof problems in captive giraffes. Acknowledgments: The authors thank Michael Stratmann and the other members of the Animal Imaging team for their technical assistance with

WAKEMAN ET AL.—MRI OF ADULT GIRAFFE’S DISTAL LIMBS WITH HOOF OVERGROWTH

the MRI system. The authors also acknowledge the staff at the Fort Worth Zoo for their support and assistance with this project.

LITERATURE CITED 1. Bush M. Giraffidae. In: Fowler ME, Miller RE (eds). Zoo and wild animal medicine. 5th ed. St. Louis (MO): W. B. Saunders Co.; 2003. p. 625–633. 2. Calle PP, Bornmann JC. Giraffe restraint, habituation, and desensitization at the Cheyenne Mountain Zoo. Zoo Biol. 1988;7:243–252. 3. Cawley R. Hoof trimming in giraffes. Int Zoo Yearb. 1975;15:227. 4. Citino SB, Bush M. Giraffidae. In: West G, Heard DJ, Caulkett N (eds.). Zoo animal and wildlife immobilization and anesthesia. Ames (IA): Blackwell Publishing Professional; 2007. p. 595–606. 5. deMarr TW, Ng’ang’a MM. Normal hoof angles and other parameters of selected African ungulates. Proc AAZV and IAAAM Joint Conf; 2000. p. 488–491. 6. Ewert HO. Remedial hoof-trimming in an adult Giraffe Giraffa camelopardalis. Int Zoo Yearb. 1965;5: 197–200. 7. Fowler ME. Hoof, nail, and claw problems in mammals. In: Fowler ME. (ed.). Zoo and wild animal

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medicine. 2nd ed. Philadelphia (PA): W. B. Saunders Co.; 1986. p. 549–556. 8. Shearer J K, Van Amstel SR. Functional and corrective claw trimming. Vet Clin North Am: Food Anim Pract. 2001;17:53–72. 9. Schilcher B, Baumgartner K, Liesegang A. Investigations on rumen and claw health of different wild ruminants related to sub-acute ruminal acidosis. In: Proc. Intern Conf Dis Zoo Wild Animals, Madrid, Spain; 2010. p. 271–275. 10. Valdes EV, Schlegel M. Advances in giraffe nutrition. In: Miller RE, and Fowler ME (eds.). Fowler’s zoo and wild animal medicine: current therapy, Volume 7. Philadelphia (PA): W. B. Saunders Co.; 2012. p. 612–618. 11. Van Amstel SR, Shearer JK. Biomechanics of weight (load) bearing and claw trimming. In: Van Amstel SR, and Shearer JK (eds.). Manual for treatment and control of lameness in cattle. Ames (IA): Blackwell Publishing Professional; 2006. p. 42–126. 12. Zuba JR. Hoof disorders in nondomestic Artiodactylids. In: Miller RE, Fowler ME (eds.). Fowler’s zoo and wild animal medicine: current therapy, Volume 7. Philadelphia (PA): W. B. Saunders Co.; 2012. p. 619– 627. Received for publication 24 June 2013