neurological examination in turtles

8/13/2019 Neurological Examination in Turtles

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eurologic ex min tion of se turtlesCheryl Chrisman, DVM, MS, EdS; Michael Walsh, DVM; John C. Meeks, DVM;

Heidi Zurawka, DVM; Richard LaRock, DVM; Larry Herbst, DVM, PhD;Juergen Schumacher, Dr Med Vet

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Objective-To determine whether neurologic exami-nation techniques established for use on pogs andcats could be adapted fo r use on sea tur tlesDesign-Prospective controlled observational studyA n i ma l s -4 healthy Green Turtles Chelonia mydas .1 h ea lt hy K em p s r id ley sea turtle Lepidochelyskemp, . and 6 Green Turtles suspected to have neu-rologic abnormalitiesProcedure--Neurologic examinations were performedwhile sea t urt le s we re in and o ut of the water and inventral and dorsal recumbency Mentation generalactivity head and body posture movement and co-ordination thoracic and pelvic l im b m ov em en tstrength and muscle tone and tail m ove me n t we reobserved Thoracic and pelvic l imb flexor reflexesand nociception righting response cranial nerve re-flexes clasp and cloacal reflexes and neck dorsalscute cloacal and ta ll nociception were testedResults-Results of neurologic evaluations were con-sistent for healthy sea turtles ea turtles suspected tohave neurologic abnormalities had abnormal resultslinic l Im plicat ions-M any of the neurologic ex-amination techniques used to evaluate dogs and catscan be adapted and used to evaluate sea turtles Astandardized neurologic examination should result in

an accurate a ssessme nt o f neurologic function inimpaired sea turtles and should help in evaluatingeffects of rehabilitation efforts and suitability fo r re-turn to their natural environment J m Vet Med ssoc1997;211:1043-1047

Two families and 7 species of sea turtles are cur . rently recognized. l The family Cheloniidae includesth e Green Turtle Chelonia mydas , HawksbillEretmochelys imbricata , Loggerhead Caretta caretta ,Kemp's r id ley sea turtle Lepidochelys kempi , Oliveridley Lepidochelys olivacea , and Flatback Cheloniadepressa . The family Dermochelyidae includes onlythe Leatherback Dermochelys coriacea . Cheloniidaeturtles have paddle-shaped thoracic l imbs, a nonretractable neck, roofed-over skull, and complete series of inframarginal scutes. The Leatherback has aunique shell structure.

From the Department of Small Animal Clinical Sciences,College of Veterinary Medicine, University of Florida, Gainesville,FL 32610-0125 Chrisman, Zurawka ; Sea World , 7007 Sea WorldDr, Orlando, FL 32821 Walsh ; Depar tment of Companion Animal and Special Species Medicine, College of Veterinary Medicine,North Carolina StateUniversity, Raleigh, NC 27606 Meeks ; TexasDiagnostic Laboratory, 1103 Winecup Ct, College Station, TX 77845LaRock ; Institute for Animal Studies, Albert Einstein College ofMedicine, Bronx, NY 10461 Herbst ; and Depar tmen t o f Comparative Medicine, College of Veterinary Medicine, University ofTennessee, Knoxville, TN 37901 Schumacher .

The authors thank Drs. Elliott Jacobson and Bruce Homerand t he s ta ff a t Sea World for assistance.

JAVMA, Vol 211, No.8, October 15, 1997

Several genera of sea turtles are on the endangeredspecies list l and, therefore, are protected by law. Evaluation by a veterinarian is necessary prior to euthanasiaeven of gravely injured sea turtles. Increased impact ofhuman activities (especially boat strikes and naturaldiseases on sea turtles results in more tur tles beingbrought into rehabili tat ion programs, where there aretremendous strains on manpower, space, time, andmonetary resources. Therefore, it is important to differentiate turtles that can recover and be released fromthose that will be permanently impaired. At least partof this process should involve an accurate evaluationof neurologic function.Because of similarities in the basic organization ofthe nervous systems in sea turtles and mammals, neurologic examination techniques developed for use indogs and cats should be applicable for turtles. Thebrain in sea turtles is linearly arranged into a forebraintelencephalon and diencephalon , midbrain mesencephalon , and hindbrain metencephalon and myelencephalon).2,3 As in mammals, there are 12 pairs of cranial nerves, and paired cranial nerve nuclei are organized, as in all vertebrates, into 4 longitudinal columns somatic motor, somatic sensory, visceralmotor,and visceral sensory nuclei extending along each sideof the midbrain, pons, and medulla oblongata. Cranialnerve nuclei are located in the same brain stem segments as they are in mammals.3,4 The cerebellum is athin flap of tissue over the caudal brain stem and contains 3 cell layers.2The gross and histologic arrangement of the spinal cord in sea turtles is similar to that in mammals. 2Enlargements are evident in the areas of the thoracicand pelvic limbs. Gray matter is divided into dorsaland ventral horns, and white matter is divided intodorsal, lateral, and ventral funiculi.Sea turt les have 8 cervical vertebrae (vs 7 in dogsand cats , 8 or 9 thoracic and lumbar vertebrae, 3 sacral vertebrae, and more than 10 caudal vertebrae Fig1). Thoracic and lumbar vertebrae are fused to thecarapace or shell and are difficult to differentiate. Female sea turt les have shorter tails than do males. Anarticulation between the dorsal process of the eighthcervical vertebra and carapace contributes to the in ability of sea turtles to retract their necks completely.This articulation contains cartilage and synovial fluid.A standardized approach to examination of thenervous system ensures that a neurologic abnormalitywill be detected and localized to a spec if ic anatomicsite and that the dysfunction can be classified as mild,moderate, or severe. A complete neurologic examinat ion o f dogs and cats can be divided into 4 sections:evaluation of the head, gait, neck and thoracic limbs,and back, pelvic limbs, tail, and anus. 5

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Figure l-Lateral radIographIc prOjections of the cervical and thoracIc IIeft) and thoracic, lumbar, sacral, and caudal right) vertebrae of a sea lunJe obtained at necropsy alier lateral sectJOns of the carapace had been removed.Notice articulaTion between C8 and the carapace, which preveniS neck retrachon ThoracIc and lumbar vertebraeare fused to the carapace and are diff icult to d fferentiate ThIs turtle had 10 thoracic and lumbar verteorae

Evaluation of Ihe head lllcludes ohser..an on s o fmentation. behavior. head posture an d coordinalion.an d cmnial nen e funclion and is useful for detectingahnorma1Jties in telencephalic. brain s tem, and cerebellar funClion. Evaluation of th e gail during walking. Irolling. galloping, and turning can be usefu l inevalualing limb coordination and strength. l\.eck an dback slrength. paslure, muscle s ize (ie. 31rophy orh}pcr l rophr) . and nociception should be obsencd.

Thoracic an d pel\ic limbs ar e evaluated h} observing response 0 wheelbarrowing an d hopping an dby Icsting for conscious proprionption 10 deleel suhtlesensor) and mOlar dysfunctions. Stretch Cie. biceps,lriceps. and extensor carpi radialis reflexes) an d fle,or(ie. withdrawal refle,) reflexes arc evaluated in Ih 'thoracic limbs. Strt lch (ie, paleliar. gastrocnemius. andcranial l ibial reflexes) alld f lexor ( ie . withdrawal reflex) r e n e x ~ an d the . >cialic nDlch response are cvalllaled in th e pelvic limbs. The eXlensor thrust renex is\ariable . but rna}' be increased with t enlral neuropaIhics an d decre.15ed \\ lth peripheral neuropathies. so itshould be evalu.ned ('d to determme which neurologic cxaminalion techniques u;:;.ed on dogs and cals \\'ould be llseful for

c v a l u a u n ~ neurologic responses m sea lunles. A neurologicc-xllmmatiOl1 was then paformed on 6 Green Tunics (L'arapace lenjl,lh, 60 to 120 cm) suspecled 10 haH neurologicahnormalil1es rour of thc 0 were suspeCied 10 haH' spinalcord lIljuriesassociated with carapace fracturcs suffrred several monlhs previously, apparenll) as a result of boat strikes.

h ~ 4..ea lunle .. all had a 'peh-ic noat body pOSItHe (ie,the caudal pari of the bod noaled hIgher in Ihe aler Ihandid the cr:lnlal part). The other sea Unles suspected 10have neurologic abnormali ties did not h a l ~ all\ ob\loussign > of mJuf)E\'alualloll of swtmming abllil)' \\as subslilUled fore\ aluanon or gall dUring e amillalion 01 sea tunks, >tcausc waler IS thei r natura l habi ta t and because onlv females spend nme on land (ollh for the shorllime neceSS4ryt,1 la) eggs) Tutlle:. were ohsencd \\-hile ther \\cre sWim-

ming In a water-fil ll'd holdmg tank and agam while Ihey\ ~ C r e tlUI of the water 011 th r woodell plalroml around thelank III \clllral and dor:;al recumbency (Fig I

OhscnlltiOllS while lunles were in the w3Ier-\lenla1l0n was 3Ssesst'd as alert (Ie. rcsponsi\'e to external sumuli).t l l p r e ~ s e d (ie, reduced. compared \\Ith normal. bUI appropriate respon:.i\enco;.. to eXlernal Slimulil. dl 'mented (ie.mappropri:llr beh.lvlOr ,delirious (ie. manic >tha\ior).SIUporous (ie. reduced con i


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Figure Checklist for neurologic examination of sea turtles.

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Turtles suspected to have neurologic abnormalit ies-The 4 turtles with carapace fractures all had pelvic l imb dysfunct ion, suggesting injury to t he thoracolumbar port ion of the spinal cord. Three turtles 1,2 and of the 4 had paraparesis, and 1 turtle 4 hadparaplegia. Of the remaining 2 turtles, 1 turtle 5 wassuspected to have cerebellar dysfunction and the otherturtle 6 was suspected to have cerebral dysfunction.Turtle 1 had paraparesis that was worse on the leftside than on the right. Flexor reflex, muscle tone andstrength, and dermal and periosteal nociception of theleft pelvic limb were reduced, compared with responsesfor the right pelvic limb. Bilateral crossed extensorreflexes were detected. The left cloacal region had reduced nociception and no clasp response. Sacral scuteand tail nociception were absent.Turtle 2 had flexor reflexes and crossed extensorreflexes in both pelvic limbs, bu t pelvic limb movement was questionable and tail movement was absent.Dermal and periosteal nociception were absent frompelvic limbs. The cloacal reflex and clasp response werepresent, but there was no cloacal, tail, or s cutenociception.Turtle 3 had paraparesis that was worse on theright side than on the left. The flexor reflexwas weakerin the r ight , compared with the left, pelvic limb, bu tdermal and per iosteal nociception were detected inboth pelvic limbs. The cloacal reflex and clasp responsewere detected. Cloacal nociception and tail movementand nociception were normal. Scute nocicept ion wasreduced beginning in the midthoracolumbar region.Turtle 4 had paraplegia with muscle contracture,absent flexor reflexes, and absent dermal and periostealnociception in both pelvic limbs and no clasp response.Pelvic limb muscl e tone could no t be accurately assessed because of muscle contr ac ture . Although theturtle had a cloacal reflex, it had no cloacal nociception,tail movement or nociception, or scute nociception.

Tur tle 5 had uncoordinated movements, tremorsof t he head, and continual horizontal nystagmus. Results of the rest of the neurologic examination wereconsistent with those for healthy turtles.Turtle 6 was demented and had reduced activity.Results of the rest of the neurologic examination wereconsistent with those for healthy turtles.iscussion

In this study, techniques adapted from those usedfor neurologic examination of dogs and cats could beused to differentiate healthy sea turtles from thosesuspected to have neurologic abnormalities. Results ofneurologic examination of healthy turtles were consistent with those for healthy dogs and cats. Increaseduse o f this standardized examination technique couldlead to the discovery of new examination techniquesand a more accurate evaluation of neurologic functionin turtles and other reptiles. 36 Variations in ambientai r and water temperatures during testing may alt erresponses. Ou r evaluations were done when ambientair temperature was approximately 35 C 95 F and wewere in the shade. Level of excitement or relaxationmay alter responses as well. All turtles were adapted toliving in the wildlife park and were used to being around

people. Thus, i t may have been easier to elicit responsesfrom them than from sea turtles in the wild. More experience is needed to determine what effect these variablesmight have on results of neurologic evaluation.

Interpretat ion of abnormal neurologic examination findings in sea tur tles may be different from interpretation of abnormal findings in dogs and cats. Fo rexample, sea tur tles that swim unevenly, leaning to Iside, may no t have dysfunction of the vestibular system, as would be suspected in dogs and cats with headtilt. Instead, the most common cause of asymmetricbuoyancy in the water in sea turtles is a mass or uneven gas accumulation in the l ungs or coelomic cavity.? Examination of sea turtles in and ou t of the watermay help differentiate leaning associated with vestibula r disease from leaning associated with lung or coelomic disease. In this study, for instance, turtle 5 hadspontaneous nystagmus, a sign usually associated withdisease of the ves tibular system. With more experience, other differences between responses of dogs andcats to neurologic tests and responses of tur tles arelikely to be discovered.

Rehabilitation centers treat many injured seaturtles. 8 9 Turtles 1 through 4 in this study had spinalcord injuries and visible wounds of the carapace, andspinal cord injur ies from motorboat strikes a re common in sea turtles.8-10 Some authors lO have stated that,i f l imb paresis or paralysis and spinal cord injury issuspected, then prognosis for recovery is poor. However, because dogs, cats, and other species can recoverfrom spinal cord inju rie s, i t is likely that some seaturt les can as well,5,l1 In fact, because of anatomic differences, reptiles may be capable of more spina l cordregeneration than are mammals.3 Turtles I through 4in this study had chronic spinal cord injuries. In seemslikely that accurate serial neurologic examinations ofsea turtles with spinal cord injuries will help to differentiate those turtles that may recover from those thatwill not. For example, i f a dog or cat has paraplegiawith loss of dermal and periosteal nociception for 1month, prognosis for recovery of function is considered hopeless.5 Further studies must be done to determine this kind of information for sea turtles.

Turtle 1 was necropsied several months after neurologiC examination, and sacral and caudal vertebraein the region of the carapace damage were found to befractured. Nerve roots could no t be seen in this regionbecause of fibrosis. In dogs and cats, traumaticsacrocaudal injuries can stretch lumbosacral nerves andcause paraparesis , as seen in t his t ur tle . Reducednociception in the left cloacal region, loss of the claspresponse, and reduced scute nociception in the lowerthoracolumbar region could have been a result of asacrocaudallesion, if the anatomy of the terminal port ion of the spinal cord in sea turtles is similar to that indogs and cats. A crossed extensor response is usuallyassociated with lesions cranial to L6 in dogs and cats.A lesion damaging the L6-S1 spinal cord segments ornerve roots in a dog or ca t will prevent detection of acrossed extensor response, even i f the spinal cord isalso damaged cranial to L6. I f the anatomy of sea turtlesis like that of dogs and cats, turtle 1, which had alesion in the sacrocaudal region, must have had some

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M, Morlock H, eds. Turtles: perspectives and research Malabar, Fla:Krieger Publishing Co, 1989;193-203.3. Bennett RA. Neurology. In: Mader ER, ed. Reptile medicineand surgery Philadelphia: WE Saunders Co, 1996;14 I 48.4. Cruce WLR, Nieuwenhuys R The cell masses in the brainstem of the turtle Testudo hermanni: a topographical and topological analysis. ] Comp Neurol 1974;156:277 306.5. Chrisman CL. Problems in small animal neurology 2nd ed.Philadelphia: Lea Febiger, 1991;41-72,397-431.6. Jacobson ER. Evaluation of the reptile patient. In: JacobsenER, Kollias GY eds. Contemporary issues in small animal practice:exotic animals New York: Churchill Livingstone Inc, 1988;1-8.7 Boyer TH. Turtles, tortoises, and terrapins. In: Mader ER,ed. Reptile medicine and surgery Philadelphia: WB Saunders Co,1996;332-336.8. Campbell TW Sea turtle rehabilitation, In: Mader ER, ed.Repti le medic ine and surgery Philadelphia: WB Saunders Co,1996;427-436.9, Schumacher J , Herbst L Jacobson ER, et al. Spinal cordinjur ie s i n mar ine turtles, in Proceedings 5 th In t Colloq PatholReptiles Amphibians 1995;231.10. Mautino M, Page CD. Biology and medicine of turtlesand tortoises. t Clin North Am Small Anim Pract 1993;23:1251-1270,

I I. Colter S Rucker NC. Acute injury to th e central nervoussystem. t Clin North Am Small Anim Pract 1988;18:545 552.

12. Dai ley MD, Fast ML, Balazas GH. Carettacola hawaiiensisN sp [Trematoda:Spirorchidae] from the green turtle, Chelonia mydasin Hawaii. ] Parasitol 1991;7:906 908

From rmchair I \ I \ rmisteadnimal ntelligence

Because human intellect outperforms that of Earth s other creatures, human beingshave smugly concluded that they are superior to all other species. Butas every veterinarianknows, the dumb in the term dumb animals means unspeaking, not stupid. So-calledinferior creatures are superior to human beings in many abilities, some ofwhich civilizedhuman beings lost long ago or never had. Humorist Will Rogers said that all people areignorant, only on different subjects. To paraphrase his remark, we might say that allcreatures are imperfect, only in different ways. some tiny creatures, genetically programmed instinct effectively substitutes forintellect. The spider engineers and constructs its flawless web of material produced fromits own body. The fragile monarch butterfly, once an earth-bound caterpillar, finds its wayacross thousands of miles from Canada to Mexico, to the same forest where its ancestorshave wintered for generations. The aging salmon leaves the sea and fights its way upstreamand over waterfalls to spawn and die in the fresh inland water where i t was born.Limited intelligence of many animals has been enhanced by extraordinary development of special senses. A dog can use its acute sense of smell to track a forest animal ora human fugitive or to sniffour hidden illicit drugs or explosives. A lost cat, through somedirectional sixth sense, can navigate hundreds ofmiles to return to its home.For all their differences, many animals share with human beings some oflife s nobler

sentiments. The dog s capacity for expressing love, loyalty, and heroism is legendary.Elephants poignantly grieve at the death of a herd member. Wild jungle cats are gentle andsolicitous toward their young. The swan has a single mate for life, setting an example offidelity that might well be emulated by more of human society.A lifetime of acquaintance with animals brings not only a better understanding ofthem, but also increased respect for their remarkable talents, instincts, and virtues. Asplayers in the grand scheme of nature, they are not inferior or incomplete, only different.And this world surely would be a far poorer place without them.

References1 Pritchard PCH. Taxonomy, evolution and zoogeography.In: Harless M, Morlock H, eds , Turtles: perspectives and researchMalabar, Fla: Krieger Publishing Co, 1989;30-39.2. Powers AS Reiner A The central nervous system. In: Harless

function remainingin the sacrocaudal spinal cord segments and nerve roots and damage to the spinal cordcranial to that site for us to be able to detect a crossedextensor reflex. However, the spinal cord cranial to thefracture site was no t evaluated at necropsy.Turtle 4 was necropsied several months after neurologic examination, and a fracture of the last 2 lumbar vertebrae was found in the area of the carapacedamage. The spinal cord could no t be identified in thisarea because of fibrotic tissue. Loss of pelvic limb reflexes and periosteal pain responses, as seen in turtle are expected in dogs and cats with similar caudallumbar lesions.Turtle 6 had dementia, and a cerebral disorder wassuspected. The turtle s condition deteriorated despitetreatment, and necropsy revealed nonsuppurative encephalitis with adult trematodes and ova in the brain.Trematode infestation is a common problem in seaturtles. 7,12

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JAVMA, Vol 211, No.8, October 15, 1997 Scientific RepOl ts Original Study 1047

neurological examination in turtles

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