Sudden death in a captive mee rkat(Suricata surica tta)w ith arterial m edial and m yocardial calcification

Laura Bongiovann,Nicola DiGirolamo,Leonardo Della Salda,Marcella Massim i,M ariarita Romanucci, Paolo SelleriFaculty of Veterinary Medicine,University of Teramo,Localit`a Piano D'Accio 6400,Teramo,ItalyClinic for Exotic Animals,Center of Veterinary Specialists,Via Sandro Giovannini 53,0037,Rome,Italy

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Sudden death in a captive mee rkat(Suricata surica tta)w ith arterial m edial and m yocardial calcification

Laura Bongiovann1*,Nicola DiGirolamo2,Leonardo Della Salda1,Marcella Massim i1,M ariarita Romanucci1, Paolo Selleri21Faculty of Veterinary Medicine,University of Teramo,Localit`a Piano D'Accio 64100,Teramo,Italy
2Clinic for Exotic Animals,Center of Veterinary Specialists,Via Sandro Giovannini 53,00137,Rome,Italy

Case report http://dx.doi.org/10.1016/j.apjtb.2016.01.009

ARTICLE INFO

Article history:

Accepted 22 Nov 2015

Available online 18 Jan 2016

Meerkat

Suricata suricatta

Arterial calci fi cation

M yocardial calci fi cation

ABSTRACT

A 1-year-old male meerkat was found dead by the owner.The animal was clinically healthy andwas regularly vaccinated for distemper virus.Necropsy revealedmultifocal to con fl uentdrywhite areas in themyocardium,pneumonia and congestivehepatopathy.A ll the other organs,including gross vessels,were macroscopically normal.The heart showed histologically large,multifocal to con fl uent areas of m ineralization of the myocardium and the wall of small coronary artery.Vascular calci fi cations were also observed in the hepatic portal tracts and kidneys arteries of small/medium sizes.The arterial lumen appeared narrowed and the wall thickened due to the calci fi cation of the tunicamedia.In veterinary medicine,arterialm ineralization is regarded as ametastatic calci fi cation,as the resultof hypercalcemia and/or hyperphosphatemia.However,today, the pathogenesis of medial artery calci fi cation in humans seems to be the results of an active process resembling embryonic osteogenesis,rather than amere passive process.

1.Introduction

Very little isknown about the pathology ofmeerkat(Suricata suricatta),small carnivores belonging to the fam ily Herpestidae, originating from the South A frica,despite these animals have gained in popularity in recentyears.They also live in captivity in numerouszoosworldw ideand they recently havebeen regarded aspetanimals,butw ith poor results,due to their aggressiveness and territoriality.The detention of meerkats as pet animals is however forbidden in several countries.Mostof the pathologies reported inmeerkats are sporadic/rare tumors in captiveanimals and infectious diseases,in particular tuberculosis and toxoplasmosis,described in both w ild and captive populations[1–7]. Three cases of cholesterol granulomas have been reported, associated w ith arterial atherosclerosis in one case[8].

2.Case report

A 1-year-oldmalemeerkat(Suricata suricatta),housed alone in an external enclosure,was found dead by the owner.No abnormalitieswere noticed regarding feeding habit or behavior the days before the death.Themeerkat was clinically healthy upon previous physical exam inations and was regularly vaccinated for distemper virus.Diet consisted of dry cat food supplemented w ith chicken breast once every two days.The meerkathad unlim ited access to drinking water.

Necropsy revealedmultifocal to con fl uentdrywhiteareasin the myocardium,also visibleatthe section of the organ(Figure1a,b). Lungs showed multifocal to coalescent areas of discoloration associated to a dark appearance and increase of consistence (pneumonia)(Figure 1c).In the liver,thereweremultifocal small whiteareas,diffused on theentire surfaceof theorgan and visible also on the cutsurface(“nutmeg liver”)(Figure 1d).A ll the other organs,including grossvessels,weremacroscopically normal.

Samples from heart,liver,lung and both kidneyswere taken and routinely fi xed in 10%neutral buffered formalin,embedded in paraf fi n wax,and 5μm-thick sections were exam ined using hematoxylin and eosin staining and visualized by lightmicroscope.In order to better visualize the presence of calcium in the tunicamedia,the alizarin staining was performed.

Figure 1.Multifocal to con fl uent dry white areas in the surface of the myocardium(a),also visible at the section of the organ(b);lungs showed multifocal to coalescent areas of discoloration associated to a dark appearance and increase of consistence(pneumonia)(c);in the liver,there weremultifocal small white areas,diffused on the entire surface of the organ and visible also on the cut surface(d).

Histological exam ination of the heart revealed large,multifocal to con fl uent areas of myocardialm ineralization.The lesions appeared as extensive and multiple areas of m ineralized lacunae(Figure 2a).The m ineralized substance appeared as a basophilic,compacted,acellular,and amorphousmaterial,w ith irregular borders(Figure 2b),surrounded by am ild tomoderate amount of fi brotic tissue(Figure 2b,asterisk).Small coronary arteries showed degeneration of themedia smoothmuscle cells (Figure 2c)with small foci of initialm ineralization(Figure 2c, arrow)and larger areas of calci fi cation expanding the wall (Figure 2d,arrow).

Vascularm ineralization was also observed in the small/medium sizes arteries of hepatic portal tracts and kidneys.Inmost of the vessels,the lumen appeared narrowed and the wall thickened due to the calci fi cation of the tunicamedia.

Figure2.Large,multifocal to con fl uentareasofmineralized lacunae in the myocardium(10×)(a);aspect of the mineralized substance:basophilic, compacted,acellular,and amorphousmaterial,w ith irregular borders(b), surrounded by a mild to moderate amount of fi brotic tissue(20×)(b, asterisk);degeneration of themedia smoothmuscle cells of small coronary arteries(c)w ith small foci of initialm ineralization(c,arrow)and larger areas of calci fi cation expanding thewall(40×)(d,arrow).

The lesions ranged from mild or early-to-severe or advanced degrees of calci fi cation.Inmore severe or advanced cases,the intimaland/oradventitial layerswerealso affected and the vessel layers could notbe distinguished.Areasof calci fi cation varied in size from small segments of calci fi ed elastic fi bers to extensive and multiple areas of m ineralized lacunae.Moderate,centrolobularhepatocyte vacuolar degeneration were also observed. In the lung,therewasamultifocalin fl ammatory in fi ltrationw ithin the alveoli and bronchiole,characterized by numerous neutrophils,admixed with fi brin and few macrophages and lymphocytes.The interstitium was alsomultifocally in fi ltrated w ith the same type of cells,associated w ithmultifocal edema.Nom ineralization was observed in the arteries of the pulmonary tissue.

3.Discussion

In the present case report,a diagnosis of arterial and myocardial calci fi cation,hepatic steatosis and bronchiolointerstitial pneumonia was made.The animal died suddenly, and neither clinical exam ination nor further investigationswere performed.The sudden death could be related to the extensive areas of myocardial necrosis,that,together w ith themultifocal vascular calci fi cation involving small and medium size arteries of different organs,were themain lesions noticed.

Arterial calci fi cation is characterized by the calcium m ineral depositionw ithin oneormore layersof thearterialvesselwall.It can occur in the tunicamedia and/or in the intima,where it is always associated w ith atherosclerosis in animals and humans [9,10].

In veterinary medicine,arterialm ineralization(calci fi cation) is frequently described,either as a dystrophic or metastatic process.Dystrophic m ineralization occurs in areas of in fl ammation,degeneration and thrombosis(notnecessarily associated to arteriosclerosis)and represents a m ineralization of necrotic tissue.M etastatic calci fi cation is the resultof hypercalcem iaand/ or hyperphosphatem ia.In animals,this situation is described during diseases such as vitam in D toxicosis,pseudohyperparathyroidism,chronic renal disease[9].No histopathological lesions were observed in the kidneys,indicating a chronic renal failure as an unlikely underlying cause of the arterial calci fi cation.Unfortunately,since the animal died suddenly, neither clinical exam ination nor further investigations were performed,and we do not know the calcem ic status of the animal,and its biochem ical pro fi le.However,we observed thatm ineralization clearly arose in the tunicamedia of smallmedium sized vessels.This condition has been described in domestic animals as the equivalent of M onckeberg's medial sclerosis of humans[9].Indeed,in human medicine,two categories of vascular calci fi cation have been described: intimal(associated w ith atherosclerotic plaques)and medial [10].The exact pathogenesis of medial artery calci fi cation in huma

ns is still poorly understood.One hypothesis is that it is the results of an active process resembling embryonic osteogenesis,in which vascular smooth-muscle cells may acquire potential biom ineralizing capabilities by undergoing osteogenic and/or chondrogenic differentiation and several proteins normally involved in bone m ineralization are also present in calci fi ed areas of the arterialwall[8].

In conclusion,arterial medial calci fi cation has been rarely described in animals.The currentcase describes the presence of dramatic m ineralization of the tunica media of small and medium-sized arteries of the heart,liver and kidney,inassociation withmyocardialm ineralization in a captivemeerkat. The cause of arterialmedial calci fi cation remains undeterm ined.

Con fl ict of interest statement

We declare thatwe have no con fl ictof interest.

Acknow ledgm ents

The authors thank Francesco Origgi for the helpful discussions on the slides and Marina Baffoni for the technicalsupport. References

[1]AiharaN,UneY.Pleomorphic liposarcomaof the intrathoraciccavity in ameerkat(Suricata suricatta).JVetMed Sci2009;71(5):685-8.

[2]Dadone LI,Garner MM,Klaphake E,Johnston MS,Han S. Anaplasticmandibular carcinoma in ameerkat(Suricata suricatta). JZoo WildlMed 2014;45(2):413-6.

[3]Singh BP,Patterson-Kane JC,Redrobe SP,Chapman JL.Intrarenal pelvic nephroblastoma in a meerkat(Suricata suricatta).J Vet Diagn Invest2005;17(6):623-5.

[4]Basso W,Mor′e G,Quiroga MA,Pardini L,Bacigalupe D, Venturini L,et al.Isolation and molecular characterization of Toxoplasma gondii from captive slender-tailed meerkats(Suricata suricatta)w ith fatal toxoplasmosis in A rgentina.Vet Parasitol 2009;161(3–4):201-6.

[5]Boonsri K,Sritan J,Vechmanus T,O'Sullivan MG,Pringproa K. Intrahepatic cholangiocarcinoma in a captive meerkat(Suricata suricatta).JZoo WildlMed 2013;44(3):740-3.

[6]Drewe JA,Foote AK,Sutcliffe RL,Pearce GP.Pathology of Mycobacterium bovis infection in w ild meerkats(Suricata suricatta).JComp Pathol 2009;140(1):12-24.

[7]Parsons SD,Drewe JA,Gey van Pittius NC,W arren RM,van Helden PD.Novel cause of tuberculosis inmeerkats,South Africa. Emerg Infect Dis 2013;19(12):2004–7.

[8]Sladky KK,Dalldorf FG,Steinberg H,W right JF,Loom is MR. Cholesterol granulomas in threemeerkats(Suricata suricatta).Vet Pathol 2000;37:684-6.

[9]M axie MG,Robinson WF.Cardiovascular system.In:Maxie MG, editor.Jubb,Kennedy,Palmer's pathology of domestic animals. Vol.3.5th ed.Edimburg:Saunders Elsevier;2007.

[10]Rocha-Singh KJ,Zeller T,Jaff MR.Peripheral arterial calci fi cation:prevalence,mechanism,detection,and clinical implications. Catheter Cardiovasc Interv 2014;83(6):E212-20.

20 Oct 2015

*Corresponding author:Laura Bongiovanni,Faculty of Veterinary M edicine, University of Teramo,Localit`a Piano D'Accio 64100 Teramo,Italy.

Tel:+39 0861 266890

E-mail:lbongiovanni@unite.it

Peer review under responsibility of Hainan M edical University.The journal implements double-blind peer review practiced by specially invited international editorial boardmembers.

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