Case Report Nasal Adenocarcinoma in a Horse with

Case ReportNasal Adenocarcinoma in a Horse with Metastasis to LungLiver and Bone and Review of Metastasis in Nine Horses withSinonasal Tumors

Ashley Hanna1 Susanne M Stieger-Vanegas1 Jerry R Heidel2 Melissa Esser1

John Schlipf1 and Jacob Mecham1

1Department of Clinical Sciences College of Veterinary Medicine Oregon State University Magruder Hall Corvallis OR 97331 USA2Department of Biomedical Sciences College of Veterinary Medicine Oregon State University Magruder Hall CorvallisOR 97331 USA

Correspondence should be addressed to Susanne M Stieger-Vanegas susannestiegeroregonstateedu

Received 14 May 2015 Revised 22 June 2015 Accepted 24 June 2015

Academic Editor Franco Mutinelli

Copyright copy 2015 Ashley Hanna et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Sinonasal neoplasia metastasizing to distant organs is rare in horses This case report describes the clinical and imaging findingsof a horse with sinonasal neoplasia which had metastasized to the lung liver and humerus Additionally the prevalence ofsinonasal neoplasia and their incidence of distantmetastasis among horses that presented to the Oregon State University VeterinaryTeachingHospital (OSU-VTH)were estimated Of 5558 equine patients who presented to theOSU-VTH in the last nine years 14were diagnosed with sinonasal disease and 103 of these cases had sinonasal neoplasia with only one having confirmed distantmetastasis This case was an eleven-year-old quarter horse which was evaluated due to a history of a right forelimb lameness ofthree weeks duration Two and a half months later he presented again this time for unilateral epistaxis and persistent right forelimblameness Radiography of the right elbow noted an increasingly irregular periosteal response and osteolytic lesion of the rightdistal humeral condyle At the time of the second presentation nasosinal endoscopy identified a lobulated mass in the region ofthe ethmoid turbinates Histopathology of this mass revealed an adenocarcinoma of nasal origin with metastasis to the lung liverand right humerus

1 Introduction

Adenocarcinomas in the horse are uncommon but have beenreported to occur in a variety of locations including lungintestine kidney skin lacrimal gland testes ovary mam-mary tissue sinuses and nasal passages [1ndash7] Adenocarci-nomas of nasal and paranasal sinus origin are rare tumorsaffecting equids but can cause significant morbidity Morecommonly the tumors originate in the maxillary area than inthe nasal area [1] They are often aggressive locally invasiveneoplasias that carry a poor prognosis [8]These tumors havebeen reported to extend from the nasal cavity and paranasalsinuses through the cribriform plate into neural tissue andoften tend to metastasize to regional lymph nodes [1 9]Distant metastases of nasal adenocarcinomas to the lunghave been described in two horses however this appears

to be a rare occurrence This is likely in part secondary tothe low number of affected animals submitted for necropsyand in part due to the limitations of the current diagnostictechniques available evaluating the horses [1 8] Thoughthere has been no evidence of equine nasal adenocarcinomametastasis to bone there are reports of intestinal and renaladenocarcinomasmetastasizing to the axial and appendicularskeleton [2 7 10]

Neoplasia involving the appendicular skeleton in horsescan cause severe lameness that is often attributed to bonepain soft tissue pathology or a nonpathologic fractureMetastatic lesions as well as primary bone neoplasia cancause significant osseous destruction which is caused by anincreased osteoclastic activity secondary to a dysregulationof the normal bone homeostasis The osseous destructionin combination with focal inflammation and increasing

Hindawi Publishing CorporationCase Reports in Veterinary MedicineVolume 2015 Article ID 845870 6 pageshttpdxdoiorg1011552015845870

2 Case Reports in Veterinary Medicine

(a) (b)

Right humerus

(c)

Figure 1 Radiographs of the right elbow at first presentation in (a) lateromedial and (b) craniocaudal views A faint lucency is noted inthe lateral aspect of the condyle of the right humerus There is mild periosteal bone proliferation on the lateral aspect of the distal humerusmetaphysis and condyle (marked by white arrow) which is best noted in the craniocaudal view (c) Ultrasound image of the lateral aspectof the condyle of the right humerus A marked irregularity of the bone surface just proximal of the origin of the lateral collateral ligament(marked by white arrow) of the right elbow joint is noted

tissue acidity results in sensitized and partially destroyedperipheral nerve endings resulting in a high level of pain [11]Osteosarcoma fibrosarcoma and chondrosarcoma involvingbone have been documented infrequently in horses In noneof these horses metastatic lesions were present at necropsysuggesting that the incidence of metastasis might also be lowin these tumor types however larger case series are neededto confirm this finding [12] This case report describes a caseof nasal adenocarcinoma with distant metastasis to multipleorgans including liver lung and the distal right humerusTo the authorsrsquo knowledge this is the only report of nasaladenocarcinoma in the horse with metastasis to bone

2 Case Presentation

An eleven-year-old quarter horse gelding used for pleasureriding first presented to the Oregon State University Vet-erinary Teaching Hospital (OSU-VTH) for a right forelimblameness of three weeksrsquo duration He had been treated withoral flunixin meglumine (Banamine Merck Animal HealthWhitehouse Station NJ USA) at a dose of 11mgkg once per

day by the owners with no improvement At presentationthe horse displayed a grade 45 right forelimb lamenesswas dragging his toe and was reluctant to further flexionof the limb On physical examination the horse stood withhis right forelimb in slight flexion and his toe pointedHe had a positive response to hoof testers on his rightforelimb Palpation of the right forelimb elicited a mild painresponse at the origin of the lateral collateral ligament of theelbow

Localized abaxial sesamoid perineural anesthesia of theright forelimb did not improve the lameness Intra-articularanesthesia of the elbow joint resulted in mild improvementbut did not resolve the lameness Radiographs of the rightelbow (Figures 1(a) and 1(b)) revealed a mild irregularityof the lateral cortex of the metaphysis of the humerus andthe epicondyle of the humerus at the origin of the lateralcollateral ligament (Figure 1(b)) Ultrasound of the origin ofthe lateral collateral ligament demonstrated irregular bonymargins at the lateral cortex of the distal humerusmetaphysisextending to the proximal aspect of the attachment of thelateral collateral ligament (Figure 1(c)) which at the time was

Case Reports in Veterinary Medicine 3

thought to be consistent with trauma secondary to injury ofthe lateral collateral ligament

The horse was sent home with instructions for stallrest administration of 22mgkg of oral phenylbutazone(Butapaste Butler Schein Animal Health Dublin OhioUSA) twice per day and application of a 510158401015840 strip of top-ical 1 diclofenac sodium (Surpass Boehringer IngelheimVetmedica St Joseph MO USA) over the right elbow jointtwice per day According to the owner the phenylbutazonewas not providing adequate analgesia and was discontinuedTherefore oral gabapentin (Neurontin Pfizer New York NYUSA) at a dose of 45mgkg twice per day and oral firocoxib(Equioxx Merial Duluth GA USA) at a dose of 01mgkgonce per day were prescribed While receiving gabapentinand firocoxib the horse became sound at the walk It wasrecommended to reevaluate the horse in two weeks or earlierif the horse was not improving with treatmentThe owner didnot schedule a visit and was contacted by phone two weeksfollowing the initial examination and reported that the horsewas still sound at walk No other concerns about the horsewere voiced at that time

Two and a half months after his initial visit the horsepresented again with a complaint of a mild intermittent leftsided epistaxis over the last two months The most recentepisode of epistaxis was more severe and longer in durationthan previously At the time of presentation the horse wasreceiving gabapentin and firocoxib at the doses previouslyprescribed On physical exam the horse had a constant dripof blood coming from his left nostril Rectal temperatureheart rate and respiratory rate were within normal limitsBlood work revealed a packed cell volume of 35 (referencerange 32ndash53) and total protein of 8 gdL (reference range57ndash79 gdL)

The day following admittance endoscopy revealed alobulated mass in the region of the left ethmoid turbinatesA biopsy of the mass was obtained and submitted forhistopathology

Radiographs of the skull (Figures 2(a) 2(b) and 2(c)) andright elbow (Figures 3(a) and 3(b)) were subsequently per-formed Radiographs of the skull revealed a poorly definedirregularly outlined soft tissue opacity in the region of theleft ethmoid turbinates (Figure 2(c)) Radiographs of theright elbow were compared to the previous radiographs andmoderate irregular periosteal proliferation at the distolateralaspect of the humerus in the location of the origin of thelateral collateral ligament of the elbowwas noted (Figures 3(a)and 3(b)) The periosteal proliferation was more pronouncedthan on the previous radiographs (Figures 1(a) and 1(b))In addition a heterogeneous lucency was present in thedistomedial aspect of the humeral condyle that was notappreciated on the previous radiographs Based on the mostrecent radiographs a healing avulsion fracture was consid-ered unlikely At this time an underlying aggressive processwas suspected with the most likely differential diagnosisbeing neoplasia and less likely osteomyelitis

Histologically the ethmoidalmass consisted of neoplasticepithelial cells arranged in tubuloacinar tubular and solidpatterns all of which were transected by bands of fibrovas-cular tissue harboring large numbers of mixed mononuclear

inflammatory cells (Figure 4) The neoplastic cells featuredmoderate anisocytosis and anisokaryosis with frequentmitotic figures Mucous-filled spaces and foci of necrosisaccompanied by neutrophilic inflammation interrupted theneoplastic cell populationsThe findings were consistent witha diagnosis of nasal adenocarcinoma

Due to multiple lesions with poor prognoses the ownerelected humane euthanasia The horse underwent a com-plete necropsy The mass in the region of the left ethmoidturbinates measured 9 times 5 times 3 cm It was attached to theturbinates near their caudal extent but did not penetratethe cribriform plate (Figure 2(d)) Dissection of the condyleof the right humerus showed areas of variable malacia(Figure 3(c)) Gross pathology in the lungs included patchyatelectasis pulmonary edema and foci of pleural thickeningThere were no gross lesions present in any other organsSamples of all major organs as well as those having visiblelesions were fixed in neutral buffered formalin for histologicexamination

Histologic features of the mass from the left ethmoidturbinates were similar to those found in the previousbiopsy and remained consistent with nasal adenocarcinoma(Figure 4(a)) The liver and lung had intravascular accumu-lations of similar clustered neoplastic epithelial cells in thelung these cells formed tubuloacinar patterns There weresimilar accumulations of epithelial cells invading the boneof the right distal humerus (Figure 4(b)) Based upon thesefindings and the absence of other potential primary tumorsa final diagnosis of nasal adenocarcinoma with metastasis toliver lung and distal humerus was made

To estimate the prevalence of sinonasal neoplasia medi-cal records of the Oregon State University Veterinary Teach-ing Hospital from July 2004 to April 2013 were reviewedfor equids diagnosed with sinonasal disease Of these equidsdiagnosed with sinonasal disease all equids with con-firmed sinonasal neoplasia were evaluated for presentingclinical signs diagnostic tests performed and imaging andhistopathologic findings Of 5558 equine patients that pre-sented to the Oregon State University Veterinary TeachingHospital in the last nine years 78 horses and one mulewere diagnosed with sinonasal disease (14 of the totalnumber of horses seen) Of these seven horses and onemule were diagnosed with a neoplasia originating in thenasal or paranasal sinus (014 of the total number of horsesseen) All of the cases with sinonasal neoplasia presentedwith nasal discharge 75 had unilateral nasal dischargeOne horse started with unilateral nasal discharge whichbecame later bilateral Only two of the cases with sinonasalneoplasia had epistaxis In these 8 cases the following otherchanges were noted facial deformities (119899 = 2 25) externallymphadenopathy (119899 = 2 25) dyspnea (119899 = 2 25) fever(119899 = 1 13) ocular discharge (119899 = 1 13) exophthalmos(119899 = 1 13) and lameness (119899 = 1 13) The followingdiagnostic tests were performed in the 8 cases of sinonasalneoplasia skull radiographs (119899 = 6 75) endoscopy (119899 = 788) sinusoscopy (119899 = 2 25) biopsies (119899 = 6 75) andnecropsy (119899 = 4 50) Histologic diagnoses of these tumorswere lymphoma (119899 = 2) adenocarcinoma (119899 = 2) andsquamous cell carcinoma osteoma respiratory transitional


(a) (b)

(c) (d)

Figure 2 Radiographs of the skull at the time of second presentation in (a) dorsoventral and (b) lateral views An indistinct soft tissueattenuating area is summating with the left turbinate region rostral to the rostral border of the choanae (c) Oblique radiographic view of theleft frontal and maxillary area An indistinct soft tissue attenuating area is noted summating with the left lateral aspect of the ethmoid area(d) Photographic image of the skull cut open in a left parasagittal plane A dark red to tan mass is noted in the left ethmoid region attachedto the caudal aspect of the turbinates The mass does not extend through the cribriform plate Fs frontal sinus

carcinoma and undifferentiated carcinoma in one case eachOf the 7 horses including the horse described in this casereport 2 had enlargement of local lymph nodes one dueto lymphoma and in the other there was no evidence ofneoplastic cells The horse described in this case report wasthe only one with confirmed distant metastasis of a sinonasalneoplasm

3 Discussion

The incidence of sinonasal tumors in the population ofequine patients seen at our facility is low and similar to thatpreviously reported [1 13 14]The horse diagnosed with nasaladenocarcinoma with metastasis to lung liver and distal

humerus was unique as the first presenting complaint wasrelated to the metastatic lesion and not the primary diseaseEpistaxis from the nasal adenocarcinoma occurred later inthe disease process and was not confirmed to be associatedwith the ongoing lameness until necropsy

Neoplasia of the paranasal sinuses and nasal cavity is arelatively rare cause of epistaxis in horses More commoncauses include exercise induced pulmonary hemorrhageguttural pouch mycosis ethmoid hematoma and trauma[15] Often the first diagnostic step in horses with suspectedsinonasal disease is endoscopy If further information regard-ing the lesion is desired radiography is traditionally usedRadiographs have proven useful for initial evaluation inhorses with sinonasal neoplasia however they are limited


(a) (b)

(c)

Figure 3 Radiographs of the right elbow at second presentation in (a) lateromedial and (b) craniocaudal view Severe osteolysis of the righthumeral condyle and marked irregularity and osteolysis of the lateral epicondyle of the right humerus are noted (c) Photographic imageof the right humeral condyle from the cranial aspect of the right humerus A large defect secondary to osseous metastasis is noted in thecentrolateral aspect of the condyle of the right humerus

(a) (b)

Figure 4 (a) Left ethmoid mass The nasal adenocarcinoma effaces normal turbinates The patterns of neoplastic cell distribution variedbetween tubular (shown) and solid Hematoxylin and eosin 400x (b) Right humerusMetastatic nasal adenocarcinoma with tubular patterninvading cortical bone Hematoxylin and eosin 100x

in their ability to localize the lesion to the correct locationIn this case radiography was the only imaging modalitydone as treatment was not pursued However in cases ofsinonasal neoplasia where surgery is warranted or furtherprognostic information is desired CT andMRI have shown tobe beneficial [16 17]The advantages of CT include the abilityto better evaluate disease extension assess involvement ofsurrounding osseous structures and more precisely localize

the disease [16] MRI has been suggested to be more accuratethan CT to determine the degree of brain involvement aswell as damage to the soft tissues surrounding the orbitA potential drawback of MRI is the intense sensitivity toinflammatory changes which could lead to over diagnosis ofa benign lesion [17]

Based on the presence of a nasal adenocarcinoma in thispatient the absence of other primary sites of adenocarcinoma


in this horse and metastatic epithelial cells invading thehumerus we present this as the first report of an adenocarci-noma of nasal or paranasal sinus originmetastasizing to bonein a horse There have been reports in horses of adenocar-cinomas originating from other sites that have metastasizedto bone causing significant lameness This includes twocases of intestinal and one of renal adenocarcinoma withmetastatic osseous involvement [2 10 18] In all of the casesof metastatic adenocarcinoma to bone the horses developeda significant lameness at some point in the disease processThis emphasizes the importance of evaluating the patientthoroughly as some clinical signs associated with the primarydisease process may easily be overlooked

This case report displays that sinonasal neoplasia inthe horse can lead to distant metastatic disease Clinicalsigns may be associated with the metastatic lesions andnot necessarily be the result of the primary tumor Thiscase also serves as a reminder that osseous neoplasia isuncommon in horses but might be a significant source oflameness Although metastatic disease associated with nasaladenocarcinoma in the horse is rare further evaluation forpresence of metastatic disease should be performed prior toinitiation of therapy

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] K W Head and P M Dixon ldquoEquine nasal and paranasalsinus tumours Part 1 review of the literature and tumourclassificationrdquo Veterinary Journal vol 157 no 3 pp 261ndash2781999

[2] M Oosterlinck E Raes S Verbraecken et al ldquoSevere lamenesscaused bymetastatic renal adenocarcinoma of the third phalanxin aWarmbloodmarerdquoEquine Veterinary Education vol 23 no10 pp 512ndash516 2011

[3] G H Edington and D F Cappell ldquoAdenocarcinoma of unde-scended testicle in the horse () secondary growths in lung andmediastinumrdquo Proceedings of the Royal Society of Medicine vol24 pp 1139ndash1140 1931

[4] F L Matheis K Birkmann M Ruetten S A Pot and B MSpiess ldquoOcular manifestations of a metastatic adenocarcinomain a horserdquoVeterinary Ophthalmology vol 16 no 3 pp 214ndash2182013

[5] F E T Pauwels S J Wigley J S Munday and W DRoe ldquoBilateral ovarian adenocarcinoma in a mare causinghaemoperitoneum and colicrdquo New Zealand Veterinary Journalvol 60 no 3 pp 198ndash202 2012

[6] G P Reppas S A McClintock P J Canfield and G F WatsonldquoPapillary ductal adenocarcinoma in the mammary glands oftwo horsesrdquo Veterinary Record vol 138 pp 518ndash519 1996

[7] J A Wright and G B Edwards ldquoAdenocarcinoma of theintestine in a horse an unusual occurrencerdquo Equine VeterinaryJournal vol 16 no 2 pp 136ndash137 1984

[8] J L Davis B C Gilger K Spaulding I D Robertson and S LJones ldquoNasal adenocarcinoma with diffuse metastases involv-ing the orbit cerebrum andmultiple cranial nerves in a horserdquo

Journal of the American VeterinaryMedical Association vol 221no 10 pp 1460ndash1463 2002

[9] J F Zaruby M A Livesey and D H Percy ldquoEthmoid adeno-carcinoma perforating the cribriform plate in the horserdquo TheCornell Veterinarian vol 83 no 4 pp 283ndash289 1993

[10] L M East P F Steyn C E Dickinson and A A Frank ldquoOccultosseousmetastasis of a colonic adenocarcinoma visualized withtechnetium tc 99m hydroxymethylene diphosphate scintigra-phy in a horserdquo Journal of the American Veterinary MedicalAssociation vol 213 pp 1167ndash1170 1998

[11] CM Kane P Hoskin andM I Bennett ldquoCancer induced bonepainrdquo British Medical Journal vol 350 article h315 2015

[12] J M Bush R L Fredrickson and E J Ehrhart ldquoEquineosteosarcoma a series of 8 casesrdquo Veterinary Pathology vol 44no 2 pp 247ndash249 2007

[13] C H Boulton ldquoEquine nasal cavity and paranasal sinus diseasea review of 85 casesrdquo Journal of Equine Veterinary Science vol5 pp 267ndash275 1985

[14] P M Dixon and KW Head ldquoEquine nasal and paranasal sinustumours part 2 a contribution of 28 case reportsrdquo VeterinaryJournal vol 157 no 3 pp 279ndash294 1999

[15] B P Smith Large Animal Internal Medicine Elsevier HealthSciences 4th edition 2008

[16] D D Cissell E R Wisner J Textor F C Mohr P V ScrivaniandA PTheon ldquoComputed tomographic appearance of equinesinonasal neoplasiardquo Veterinary Radiology and Ultrasound vol53 no 3 pp 245ndash251 2012

[17] C Tessier A Bruhschwein J Lang et al ldquoMagnetic resonanceimaging features of sinonasal disorders in horsesrdquo VeterinaryRadiology and Ultrasound vol 54 no 1 pp 54ndash60 2013

[18] H W Jann M A Breshears R W Allison et al ldquoOccultmetastatic intestinal adenocarcinoma resulting in pathologicalfracture of the proximal humerusrdquo Equine Veterinary Journalvol 41 no 9 pp 915ndash917 2009

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Case Reports in Veterinary Medicine


(a) (b)

Right humerus

(c)

Figure 1 Radiographs of the right elbow at first presentation in (a) lateromedial and (b) craniocaudal views A faint lucency is noted inthe lateral aspect of the condyle of the right humerus There is mild periosteal bone proliferation on the lateral aspect of the distal humerusmetaphysis and condyle (marked by white arrow) which is best noted in the craniocaudal view (c) Ultrasound image of the lateral aspectof the condyle of the right humerus A marked irregularity of the bone surface just proximal of the origin of the lateral collateral ligament(marked by white arrow) of the right elbow joint is noted

tissue acidity results in sensitized and partially destroyedperipheral nerve endings resulting in a high level of pain [11]Osteosarcoma fibrosarcoma and chondrosarcoma involvingbone have been documented infrequently in horses In noneof these horses metastatic lesions were present at necropsysuggesting that the incidence of metastasis might also be lowin these tumor types however larger case series are neededto confirm this finding [12] This case report describes a caseof nasal adenocarcinoma with distant metastasis to multipleorgans including liver lung and the distal right humerusTo the authorsrsquo knowledge this is the only report of nasaladenocarcinoma in the horse with metastasis to bone

2 Case Presentation

An eleven-year-old quarter horse gelding used for pleasureriding first presented to the Oregon State University Vet-erinary Teaching Hospital (OSU-VTH) for a right forelimblameness of three weeksrsquo duration He had been treated withoral flunixin meglumine (Banamine Merck Animal HealthWhitehouse Station NJ USA) at a dose of 11mgkg once per

day by the owners with no improvement At presentationthe horse displayed a grade 45 right forelimb lamenesswas dragging his toe and was reluctant to further flexionof the limb On physical examination the horse stood withhis right forelimb in slight flexion and his toe pointedHe had a positive response to hoof testers on his rightforelimb Palpation of the right forelimb elicited a mild painresponse at the origin of the lateral collateral ligament of theelbow

Localized abaxial sesamoid perineural anesthesia of theright forelimb did not improve the lameness Intra-articularanesthesia of the elbow joint resulted in mild improvementbut did not resolve the lameness Radiographs of the rightelbow (Figures 1(a) and 1(b)) revealed a mild irregularityof the lateral cortex of the metaphysis of the humerus andthe epicondyle of the humerus at the origin of the lateralcollateral ligament (Figure 1(b)) Ultrasound of the origin ofthe lateral collateral ligament demonstrated irregular bonymargins at the lateral cortex of the distal humerusmetaphysisextending to the proximal aspect of the attachment of thelateral collateral ligament (Figure 1(c)) which at the time was













(a) (b)

(c) (d)



3 Discussion





(a) (b)

(c)


(a) (b)










References



























Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of


















(a) (b)

(c) (d)



3 Discussion





(a) (b)

(c)


(a) (b)










References



























Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







(a) (b)

(c) (d)



3 Discussion





(a) (b)

(c)


(a) (b)










References



























Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







(a) (b)

(c)


(a) (b)










References



























Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of











References



























Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of













Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of






Documents

Case Report Nasal Adenocarcinoma in a Horse with