Advertisement

Comparative Clinical Pathology

, Volume 27, Issue 1, pp 135–145 | Cite as

Subclinical nodular goiter associated with Hurthle cell, papillary, and adenomatoid hyperplasic nodules in the dromedary camel in the Sultanate of Oman

  • Mohamed H. Tageldin
  • Hassan Abu DamirEmail author
  • Mansour F. Hussein
  • Elhag A. Omer
  • Mahmoud A. Ali
  • Adam M. Adam
  • Remya R. Nir
Original Article
  • 93 Downloads

Abstract

Goiter and other iodine deficiency disorders (IDD) are a worldwide problem. IDD prevalence rate of 52.7% has been reported among school children aged 9–12 years in Dhofar region, (WHO 2006) which resides adjacent to the Arabian Sea in the Sultanate of Oman. In a preliminary survey, 39.5 and 44.7% of the dromedary camels in the region exhibited low total T3 and total T4, respectively. An abattoir survey was carried out and the dromedary camels examined during the anti-mortem were clinically normal. Post-mortem examination of both thyroid lobes of slaughtered camel, revealed normal weight but 69.5% of these showed nodules of various sizes, numbers, shapes, colors and consistency in the capsular region and or deeply embedded in thyroid tissue. A wide range of histopathological changes were seen and categorized according to the dominant histological pattern into Hurthle cell nodules, papillary hyperplastic nodules, adenomatoid hyperplastic nodules and nodular colloid goiter only. The Hurthle cell nodules were either solid encapsulated cords or follicular variants of well-encapsulated macrofollicles and microfollicles of different sizes and shapes, and the Hurthle cells were seen lining the colloid follicles or forming the solid cords. In the papillary hyperplastic nodules, majority of cases lack capsule, the fronds were multiple and variable, and usually do not compress the surrounding parenchyma. Adenomatoid hyperplastic nodules formed of encapsulated follicular nodules with various sizes and shapes and containing little or no colloid. The nodular colloid goiter along with the papillary hyperplastic nodules had psammoma-like bodies without lamellation. No evidence was found of capsular or vascular invasion apart from one case which showed limited vascular and capsular invasion. The histopathology and immunohistochemistry using specific thyroid tumor markers did not reveal malignancy in all suspected cases. Total and free serum T3 and T4 and serum selenium were comparatively low, and CK enzyme was high in affected camels. The causes of the subclinical nodular goiter, probably multifactorial, were discussed.

Keywords

Dromedary camels Subclinical nodular goiter Hurthle cells Papillary hyperplasia Adenomatoid nodules Thyroid tumor markers Thyroid hormones Selenium Enzymes 

Notes

Acknowledgements

We would like to express our appreciation and gratitude for professor A.M. El Hassan, Faculty of Medicine, University of Khartoum for the second opinion; Abu Dhabi Food Control Authority, for the approval to use Al Qattara Veterinary Lab facilities; the staff in Salalah Veterinary Hospital for the help during specimen collection; the staff in the Pathology Department College of Medicine and Health Sciences, Sultan Qaboos University, Sultanate of Oman for the help in the preparation and staining of the slides; the Department of Defense Armed Forces Institute of Pathology, Washington DC, for the second opinion in some tumor markers; and the UAE University lab staff for some specimens analysis.

Funding information

This study was funded by College of Agricultural and Marine Sciences, Sultan Gaboos University, Sultanate of Oman (grant number IG/AGR/ANVS/10/01).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Abdel Gadir WS, Adam SEI (1999) Development of goiter and enterohepatonephropathy in Nubian goats fed with pearl millet (Pennisetum typhoides). Vet J 157:178–185CrossRefGoogle Scholar
  2. Abu Damir A, Barri MES, Tageldin MH, Idris OF (1990) Clinical and subclinical colloid goiter in adult camels (Camelus dromedarius) at Kordofan Region of the Sudan. Br Vet J 146:219–227CrossRefGoogle Scholar
  3. Al-Mishakhi MSA, Koll EHBA (2007) Country pasture/forage resource profile. Oman, FAO Technical Report, 23 pGoogle Scholar
  4. ANON (1992) Soil survey and land classification project, OMA/87//011.Salalah integrated study: farming survey report. Ministry of Agriculture and Fisheries, SOO, and FAO, Muscat, pp 82Google Scholar
  5. Barri MES, Al-Sultan SI (2007) Studies on Selenium and Vitamin E status of young Megheem dromedary camels at Al-Hasa province. J Camel Pract Res 14:51–53Google Scholar
  6. Beckett GJ, Beddows SE, Morrice PC, Nicol F, Arther JA (1987) Inhibition of hepatic type-1 iodothyronine deiodination of thyroxin caused by selenium deficiency in rats. Biochem J 248:443–447CrossRefGoogle Scholar
  7. Beckett GJ, Nicol F, Rae PW, Beech S, Guo Y, Arther JA (1993) Effects of combined iodine and selenium deficiency on thyroid hormone metabolism in rats. Am J Clin Nutr 57(Supplement):240S–243SCrossRefGoogle Scholar
  8. Bogin E (2000) Clinical pathology of camelides: present and future. Revue Med Vet, 151:563–568Google Scholar
  9. Bourdoux P, Delange F, Gerald M (1978) Evidence that cassava ingestion increase thiocyanate formation: A possible etiologic factor in endemic goiter. J Clin Endocrinol Metab 4:613–621CrossRefGoogle Scholar
  10. Braund KG, Dillon AR, August JR, Ganjam VK (1981) Hypothyroid myopathy in two dogs. Vet Pathol 18:589–598CrossRefGoogle Scholar
  11. Capen CC (1978) Tumors of the endocrine glands. In: Moulton JE (ed) Tumors in domestic animals, 2nd edn. University of California Press, Berkeley, Los Angeles, London, pp 372–429Google Scholar
  12. Decker RH, Hruska JC, McDermid AM (1979) Colloid goiter in a newborn camel and an aborted foetus. J Am Vet Med Assoc 175:968–969PubMedGoogle Scholar
  13. Deepa TK, Krishnaraj U (2014) Histopathological features of papillary thyroid carcinoma with special emphasis on the significance of nuclear features in their diagnosis. Arch Med Health Sci 2:16–22CrossRefGoogle Scholar
  14. Doige CE, Mclaughlin BG (1981) Hyperplastic goiter in new born foals in Western Canada. Can Vet J 22:42–45PubMedPubMedCentralGoogle Scholar
  15. Drutel A, Archambeaud F, Caron P (2013) Selenium and thyroid gland. Clin Endocrinol 78:155–164CrossRefGoogle Scholar
  16. El-Sheikh MA (2013) Weed vegetation ecology of arable land in Salalah, Southern Oman. Saudi J Biol Sci 20:291–304CrossRefGoogle Scholar
  17. Faye B, Seboussi R (2009) Selenium in camel - A review. Nutrients, 1:30–49Google Scholar
  18. Hamliri A, Khallaayoune K, Johnson DW, Kessabi M (1990) The relationship between concentration of the selenium in the blood and the activity of glutathione peroxidase in the erythrothytes of the dromedary camels (camelus dromedaries). Vet Res Commun 14:27–30CrossRefGoogle Scholar
  19. Harijoko A, Warmada IW, Sudargo T, Widagdo D, Watanabe K (2002) Factor controlling iodine deficiency disorders (IDD) incident in communities living within volcanic landscape www.cprm.gov.br/331GC/12872.htm
  20. Jubb KVF, Kennedy PC, Palmer N (1985) Pathology of domestic animals, vol 3, 3rd edn. Academic Press, New YorkGoogle Scholar
  21. Karmarkar MG, Deo MG, Kochupillai N, Ramalingaswami V (1974) Pathophysiology of Himalayan endemic goiter. Am J Clin Nutr 27:96–103CrossRefGoogle Scholar
  22. Kathleen TM, Zubair WB (2008) The thyroid Hurthle (Oncocytic) cell and its associated pathologic conditions. Arch Pathol Lab Med 132:1241–1250Google Scholar
  23. Lee MJ, Kim EK, Kwak JY, Kim MJ (2009) Partially cystic thyroid nodules on ultrasound. Probability of malignancy and sonographic differentiation. Thyroid 19:341–346CrossRefGoogle Scholar
  24. Madeiros-Neto G (2013) Multinodular goiter www.thyroidmanager.org, chapter 17
  25. McKeran RO, Lavin GS, Andrews MT, Ward P, Mair WGP (1975) Muscle fibre type changes in thyroid myopathy. J Clin Path 28:659–663CrossRefGoogle Scholar
  26. Ministry of Agriculture, Oman (MOA) (2008) The state of plant genetic resource for food andagriculture in Oman. Report 1–34. http://www.fao.org/docrep/013/i1500e/Oman.pdf
  27. Nazifi S, Mansourian M, Nikahval B, Razavi SM (2009a) The relationship between serum level and thyroid hormones, trace elements and antioxidant enzymes in dromedary camels (Camelus dromedarius). Trop Anim Health Prod 41:129–134CrossRefGoogle Scholar
  28. Nazifi S, Nikahval B, Mansourian M, Razavi SM, Farshneshani F et al (2009b) Relationships between thyroid hormones, serum lipid profile and erythrocyte antioxidant enzymes in clinically healthy camels (Camelus dromedarius). Revue Med Vet 160:3–9Google Scholar
  29. Ong CB, Thomas HH, Scott DF (2014) Hyperplastic goiter in two adult dairy cows. J Vet Diagn Investig 26:810–814CrossRefGoogle Scholar
  30. Rasmussen LB, Schomburg L, Kohrle J, Pedersen IB, Hollenbach B, Hog A, Oversen L, Perrild H, Laurberg P (2011) Selenium status. Thyroid volume and multiple nodule formation in an area with mild iodine deficiency. Eur J Endocrinol 164:585–590CrossRefGoogle Scholar
  31. Rejeb A, Amara A, Rezeigui H, Crespeau F, De Lverdier M (2012) Pathological and hormonal study of the goiter in the dromedary (Camelus dromedarius) in South of Tunisia. Revue Med Vet 163:242–249Google Scholar
  32. Rosai J, Kuhn E, Carcangiu ML (2006) Pitfalls in thyroid tumor pathology. Histopathology 49:107–120CrossRefGoogle Scholar
  33. Saeed A, Khan IA, Hussein MM (2009) Changes in biochemical profile of pregnant camels (Camelus dromedarius) in term. Comparative Clinical Pathology, 18:139–143Google Scholar
  34. Saeb M, Baghshani H, Nazifi S, Saeb S (2010) Physiological response of dromedary camels to road transportation in relation to circulating levels of cortisol, thyroid hormones and some serum biochemical parameters. Trop Anim Health Prod 42:55–63CrossRefGoogle Scholar
  35. Saikat SQ, Carter JE, Mehra A, Smith B, Stewart A (2004) Goiter and environmental iodine deficiency in the UK-Derbyshire. A review. Environ Geochem Health 26:395–401CrossRefGoogle Scholar
  36. Samir M, El-Awady MY (1998) Serum Selenium levels in multinodular goiter. Clin Otolaryngol Allied Sci 23:512–514CrossRefGoogle Scholar
  37. Suster S (2006) Thyroid Tumors with a follicular growth pattern: problems in differential diagnosis. Arch Pathol Lab Med 130:984–988PubMedGoogle Scholar
  38. Tageldin MH, ElSawi ASA, Ibrahim SG (1985) Observation on colloid goiter of dromedary camels in the Sudan. Rev Elev Med Vet Pays Trop 38:394–397PubMedGoogle Scholar
  39. Tageldin MH, Abu Damir H, Omer EA, Ali MA, Adam AM (2016) Follicular adenoma associated with spindle cell proliferation, papillary adenoma and colloid goitre in a dromedary camel. Comp Clin Pathol 25:241–245CrossRefGoogle Scholar
  40. Tajik J, Sazmand A, Moghaddam SHH, Rassoli A (2013) Serum concentrations of thyroid hormones, cholesterol and triglyceride, and their correlations together in clinically healthy camels (Camelus dromedarius): effects of season, sex and age. Vet Res Forum 4:239–243PubMedPubMedCentralGoogle Scholar
  41. Vargas-Uricoechea H, Bonelo-Perdomo A, Sierra-Tares CH (2016) Iodine and the thyroid. In: Imam SK, Ahmad SI (eds) Thyroid Disorders. Basic Science and Clinical Practice. Springer, Netherland, pp 27–48Google Scholar
  42. Vitovec J (1976) Statistical data on 370 cattle tumors collected over the years 1964-1973 in South Bohemia. Zentralbl Veterinarmed A 23:445–453CrossRefGoogle Scholar
  43. WHO (2006) Vitamin and Mineral Nutrition Information System (VMNIS) World global data base on iodine deficiency World Health Organization, Geneva, Switzerland, www.who.int/vmnis/database/iodine/countries/en
  44. Wikipedia (2016) Hurthle cell, http://en.wikipedia .org
  45. Zubair WB, Virginia AL (2002) Etiology and significance of the “optically clear nucleus”. Endocr Pathol 13:289–299CrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd. 2017

Authors and Affiliations

  1. 1.Department of Animal and Veterinary Sciences, College of Agricultural and Marine SciencesSultan Qaboos UniversityMuscatSultanate of Oman
  2. 2.Al AinUnited Arab Emirates
  3. 3.Research and Development DepartmentARASCORiyadhKingdom of Saudi Arabia
  4. 4.Veterinary Laboratory, The Department of AgricultureAbu Dhabi Food Control AuthorityAl AinUnited Arab Emirates
  5. 5.College of MedicineUAE UniversityAl AinUnited Arab Emirates
  6. 6.Laboratories and Animal Research Centre, Directorate General of Veterinary Services, Royal CourtMuscatOman
  7. 7.Faculty of Biochemistry and Molecular MedicineUniversity of OuluOuluFinland

Personalised recommendations