oronasal fistula in a 53-year-old hippopotamus: (hippopotamus amphibius)

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J. Comp. Path. 2007, Vol. 137, 253^255 SHORT PAPER Oronasal Fistula in a 53-year-old Hippopotamus (Hippopotamus amphibius) P. Wittschen, A. Ochs * and A. D. Gruber Department ofVeterinary Pathology, Freie Universitaet Berlin, Robert-von-Ostertag-Strasse 15, 14163 Berlin, and * Zoological Garden Berlin, Hardenbergplatz 8, 10787 Berlin, Germany Summary An oronasal ¢stula is described in a 53-year-old captive hippopotamus, the animal having shown a nasal dis- charge, consisting mainly of food particles, during and after feeding for at least15 years. Necropsy of the emaciated animal revealed an oronasal ¢stula, measuring 4.5 Â 3.5 cm, adjacent to the third left molar tooth, the ¢rst and second molars being missing.The ¢stula was thought to have been caused by an earlier necrotizing alveolitis and osteitis.There was no evidence of rhinitis or aspiration pneumonia. Unrelated ¢ndings consisted of a follicular thyroid adenoma and generalized muscle atrophy. r 2007 Elsevier Ltd. All rights reserved. Keywords: hippopotamus; Hippopotamus amphibius; oronasal ¢stula; periodontitis; thyroid adenoma; tumour Reports on diseases of hippopotamuses are scarce and those on dental disease completely lacking. Oronasal ¢stula has been described in human beings (Murrell et al ., 2001 ) and small animals (de Souza et al ., 2005 ), especially dogs (Welch and Swaim, 2003 ), but it is rarely documented in large animals. There are no re- cords of its occurrence in wild animals except for one report of an oronasal ¢stula in a coatimundi (Grabe- man et al ., 1982 ). Although breeding well in captivity, the common hippopotamus (Hippopotamus amphibius) has since 2006 been listed as a vulnerable species (IUCN Red List of Threatened Species) in its natural habitat in sub-Saharan Africa (Miller, 2003 ). A 53-year-old female hippopotamus in a zoo, which was bred and reared in captivity, had shown a dis- charge from the left nostril during and after feeding for at least 15 years, the discharge being composed mainly of food particles and seromucoid £uid. For most of this period the discharge did not appear to a¡ect the clinical condition or well being of the animal. Even- tually, however, in spite of good food intake, the animal began to show a weight loss, which became severe, amounting after a few months to ca 1000 kg (from a for- mer body weight of 1800 kg).This was accompanied by increasing lethargy and loss of status as group leader, the animal entering the water basin only at night when its companions remained on dry land. Probably due to decreased activity, numerous decubital ulcers devel- oped on the limbs.When the animal was humanely de- stroyed, it weighed only 600 kg. At necropsy, emaciation and general muscle atrophy were noted, together with multifocal ulcerative derma- titis at pressure points on the limbs. An oval-shaped or- onasal ¢stula measuring ca 4.5 Â 3.5cm was found in the palatal bone (Figs 1^3 ), adjacent to the 3rd left mo- lar tooth, the ¢rst and second molars and the second premolar being missing.The edges of the chronic per- forating lesion were markedly thickened in both the oral and nasal cavities. The ¢stula was densely ¢lled with grass particles up to 20 cm in length. Histological examination revealed a severe chronic necrotizing gin- givitis and alveolitis with associated chronic lytic ostei- tis and osteomyelitis. A second ¢nding was a partly cystic, well-demarcated thyroid adenoma in the cranial thoracic aperture, measuring ca 20 Â16 Â12 cm (Fig. 4 ). Histologically, the tumour presented as a www.elsevier.com/locate/jcpa ARTICLE IN PRESS 0021-9975/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi: 10.1016/j.jcpa.2007.06.009 Correspondence to: A. D. Gruber (e-mail: [email protected])

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Page 1: Oronasal Fistula in a 53-year-old Hippopotamus: (Hippopotamus amphibius)

ARTICLE IN PRESS

J. Comp. Path. 2007,Vol.137, 253^255

0021-9975/$ - see fdoi:10.1016/j.jcpa.

Correspondence to

SHORT PAPER

Oronasal Fistula in a 53-year-old Hippopotamus(Hippopotamus amphibius)

www.elsevier.com/locate/jcpa

P. Wittschen, A. Ochs* and A. D. Gruber

Department ofVeterinary Pathology, Freie Universitaet Berlin, Robert-von-Ostertag-Strasse 15, 14163 Berlin, and*Zoological Garden Berlin, Hardenbergplatz 8, 10787 Berlin, Germany

Summary

An oronasal ¢stula is described in a 53-year-old captive hippopotamus, the animal having shown a nasal dis-charge, consistingmainly of foodparticles, duringandafter feeding for at least15 years. Necropsy of the emaciatedanimal revealed an oronasal ¢stula, measuring 4.5�3.5 cm, adjacent to the third left molar tooth, the ¢rst andsecond molars being missing.The ¢stulawas thought to have been caused by an earlier necrotizing alveolitis andosteitis. There was no evidence of rhinitis or aspiration pneumonia. Unrelated ¢ndings consisted of a follicularthyroid adenoma and generalized muscle atrophy.

r 2007 Elsevier Ltd. All rights reserved.

Keywords: hippopotamus;Hippopotamus amphibius; oronasal ¢stula; periodontitis; thyroid adenoma; tumour

Reports on diseases of hippopotamuses are scarce andthose on dental disease completely lacking. Oronasal¢stula has been described in human beings (Murrellet al., 2001) and small animals (de Souza et al., 2005),especially dogs (Welch and Swaim, 2003), but it israrely documented in large animals. There are no re-cords of its occurrence in wild animals except for onereport of an oronasal ¢stula in a coatimundi (Grabe-man et al., 1982). Although breeding well in captivity,the common hippopotamus (Hippopotamus amphibius)has since 2006 been listed as a vulnerable species(IUCN Red List of Threatened Species) in its naturalhabitat in sub-Saharan Africa (Miller, 2003).A 53-year-old female hippopotamus in a zoo, which

was bred and reared in captivity, had shown a dis-charge from the left nostril during and after feedingfor at least 15 years, the discharge being composedmainly of food particles and seromucoid £uid. Formostof this period the discharge did not appear to a¡ect theclinical condition or well being of the animal. Even-tually, however, in spite of good food intake, the animalbegan to show a weight loss, which became severe,

ront matter2007.06.009

: A. D. Gruber (e-mail: [email protected])

amounting after a fewmonths to ca1000 kg (from a for-mer body weight of 1800 kg).This was accompanied byincreasing lethargy and loss of status as group leader,the animal entering the water basin only at night whenits companions remained on dry land. Probably due todecreased activity, numerous decubital ulcers devel-oped on the limbs.When the animal was humanely de-stroyed, it weighed only 600 kg.At necropsy, emaciation and general muscle atrophy

were noted, together withmultifocal ulcerative derma-titis at pressure points on the limbs. An oval-shaped or-onasal ¢stula measuring ca 4.5�3.5 cm was found inthe palatal bone (Figs1^3), adjacent to the 3rd left mo-lar tooth, the ¢rst and second molars and the secondpremolar being missing. The edges of the chronic per-forating lesion were markedly thickened in both theoral and nasal cavities. The ¢stula was densely ¢lledwith grass particles up to 20 cm in length. Histologicalexamination revealed a severe chronic necrotizing gin-givitis and alveolitis with associated chronic lytic ostei-tis and osteomyelitis. A second ¢nding was a partlycystic, well-demarcated thyroid adenoma in the cranialthoracic aperture, measuring ca 20�16�12 cm(Fig. 4). Histologically, the tumour presented as a

r 2007 Elsevier Ltd. All rights reserved.

Page 2: Oronasal Fistula in a 53-year-old Hippopotamus: (Hippopotamus amphibius)

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Fig. 1. Oral cavity. Oronasal ¢stula ¢lled with grass particles. Bar,1cm.

Fig. 2. Macerated skull (complete). Oronasal ¢stula (arrow) in thepalatal bone next to 3rd left molar tooth. Bar,7.5 cm.

Fig. 3. Palatal bone (magni¢cation from Fig. 2). View through the¢stula into the nasal cavity. Bar,1.5 cm.

Fig. 4. Thyroid adenoma. Bar, 2 cm.

P. Wittschen et al.254

follicular adenoma which, on immunohistochemicalexamination by the avidin^biotin complex method,was labelled by antibody against thyroglobulin(A 0251; Dako, Glostrup, Denmark). A mild bilateral

ventricular dilatationwas present in the heart, withouthistologically detectable myocardial changes. Thelungs showed severe anthracosis and mild interstitialand subpleural ¢brosis. No ovarian functional struc-tures were detectable in either ovary and the uterinemucosa showed no signi¢cant changes. The mesome-trial blood vessels showed marked hypertrophy ofthe arterial media and a severe subintimal ¢brosis.The mammary gland was fully involuted. The centralnervous system showed mild di¡use neuronal storageof lipofuscin. All other organs were normal, bothmacroscopically and histologically.The oronasal ¢stula, which was considered an unu-

sual ¢nding, was attributed to chronic in£ammation ofthe periodontal tissue. Moreover, the loss of two molarteeth probably occurred as a result of periodontalin£ammation and destruction of the periodontium.Oronasal ¢stulas have been described previously ascomplications of periodontal disease (Hennet, 2001).Among domestic animals, dogs of small breedsare most commonly a¡ected, usually at the site of thecanine tooth or upper fourth premolar tooth (Hennet,2001). Oronasal ¢stulas are also thought to result fromtrauma (Welch and Swaim, 2003; de Souza et al., 2005),necrosis produced by vascular disease (Gertner andHamlar, 2002), local in£ammation (Jayasankar et al.,2004) or neoplasia (Sullivan and Parente, 2003). Ascomplications, rhinitis (Marretta, 1992) or occasion-ally aspiration pneumonia (Sullivan and Parente,2003) may result from oronasal displacement of foodparticles; however, neither complication was seen inthe present study. Perhaps surprisingly, colonization ofthe nasal cavity by oral bacteria appears to result onlyrarely from oronasal ¢stula (Brennan et al., 2003). Inthe hippopotamus described here, it is surmised thatthe disease process began with periapical in£amma-tion of a tooth, caused, for example, by foreign body

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Oronasal Fistula in a Hippopotamus 255

penetration, leading to periodontitis and destruction ofadjacent bone and ¢nally to oro¢stula. The lack of as-piration pneumonia or other forms of lung disease sug-gested that the animal had learned to cope with the¢stulawithout inhaling food particles.The thyroid adenoma was considered to be unre-

lated to the oronasal ¢stula. The generalized muscleatrophy and emaciation may have been due in part tothe thyroid adenoma and in part to ageing. Althoughhippopotamuses are long-lived, neoplasia would ap-pear to be uncommon (Miller, 2003), the only previousreports being those of a pheochromocytoma (Duncanet al., 1994) and a uterine leiomyoma (Miller, 2003) inthe common hippo, andabenign oral osteoma in apyg-my hippo (Choeropsis liberiensis) (Weston et al.,1996).Surprisingly, the present study failed to detect any le-

sions, includingdegenerative changes, in the uterus andmammary glands of the animal, despite the 20 o¡-spring to which it had given birth (Blaszkiewitz, 2006).This accordedwith the clinical observation that the an-imal remained fertile until the end of its life, necessitat-ing administration of oral contraceptives during the¢nal 12 months to prevent pregnancy, which wouldotherwise have exacerbated the deteriorating bodycondition.

References

Blaszkiewitz, B. (2006). Additional information on hippohusbandry in the Zoological Garden Berlinç1st supple-ment. In: Contribution to theAnimalHusbandry andAnnual Re-

port of the Zoological Garden Berlin,Vol. 36, J. Lange and H.Kloes, Eds, Zoological Garden Berlin, Berlin, Germany,pp. 63^66.

Brennan, P. A.,Willy, P., Anand, R. andMarkus, A. F. (2003).Colonization of the cleft nasal £oor by anaerobic oral£ora in patients with oronasal ¢stulae. Cleft Palate Cranio-facialJournal, 40, 431^432.

de Souza, H. J., Amorim, F.V., Corgozinho, K. B. and Ta-vares, R. R. (2005). Management of the traumatic orona-sal ¢stula in the cat with a conical silastic prostheticdevice. Journal of FelineMedicine and Surgery, 7,129^133.

Duncan, M., Grahn, B. H. andWilcock, B. P. (1994). Pheo-chromocytoma associated with hypertensive lesions in ariver hippopotamus (Hippopotamus amphibius). Journal ofZoo andWildlifeMedicine, 25, 575^579.

Gertner, E. and Hamlar, D. (2002). Necrotizing granuloma-tous vasculitis associatedwith cocaine use. Journal ofRheu-matology, 29,1795^1797.

Grabeman,T. A., Davis,W. J., Hardin, C. J. and Cli¡ord, D.H. (1982). Malocclusion and oronasal ¢stula in a coati-mundi: treatment by an endodontic procedure. Journal ofAmericanVeterinaryMedical Association, 181,1403^1405.

Hennet, P. (2001). Oronasal ¢stula andpalatal repair. In: Pro-ceedings of the 26th Congress of theWorld Small AnimalVeterinary

Association,Vancouver, p.15.Jayasankar, P. P., Chavda, J. and Shah, R.M. (2004). Orona-

sal ¢stula of infective origin and alveolar necrosis ina 13 year old boy. Indian Journal of Dental Research, 15,107^109.

Marretta, S. M. (1992). Chronic rhinitis and dental disease.Veterinary Clinics of North America: Small Animal Practice, 22,1101^1117.

Miller, M. A. (2003). Hippopotamidae (Hippopotamus).In: Zoo and Wild Animal Medicine, M.E. Fowler andR.E. Miller, Eds, W. B. Saunders, St Louis, Missouri,pp.602^612.

Murrell, G. L., Requena, R. and Karakla, D.W. (2001). Oro-nasal ¢stula repair with three layers. Plastic and Reconstruc-tive Surgery, 107,143^147.

Sullivan, E. K. and Parente, E. J. (2003). Disorders of thepharynx.Veterinary Clinics of North America: Equine Practice,19,159^167.

Welch, J. A. and Swaim, S. F. (2003). Nasal and facial recon-struction in a dog following severe trauma. Journal of theAmerican Animal Hospital Association, 39, 407^415.

Weston, H. S., Fagella, A. M., Burt, L., Crowley, K. andMoore,T. (1996). Immobilization of a pygmy hippopota-mus (Choreopsis liberiensis) for the removal of an oral mass.In: Proceedings of theAnnualMeetingof theAmericanAssociation

of ZooVeterinarians, PuertoVallarta, pp. 576^581.

Received, December 4th, 2006

Accepted, June 28th, 2007

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