Euthyroid Sick Syndrome and Changes in Thyroid Hormones in Dogs with Hemoparasitosis
Background: Hemoparasitoses are extremely important in the clinical routine because they affect a large number of dogs. In spite of the abundance of studies on this topic, hormonal alterations caused by infection with these agents are still poorly known. Therefore, the goal of this work was to assess the serum levels of thyroid hormones of dogs infected with Ehrlichia canis (E. canis) alone, and dogs infected with E. canis and Babesia canis vogeli (B. vogeli) and/or Anaplasma platys (A. platys) before and after treatment with doxycycline chlorohydrate. This study also aimed at checking for presence of euthyroid sick syndrome (ESS) in these animals.
Materials, Methods & Results: The concentrations of the thyroid hormones total triiodothyronine (TT3), total tetraiodothyronine (TT4), free tetraiodothyronine (FT4), and canine thyroid-stimulating hormone (cTSH) were assessed by chemiluminescence in 12 dogs. Nested polymerase chain reaction (nPCR) was used to confirm diagnoses. The dogs were divided into 2 groups: G1, which comprised animals infected by E. canis alone, and G2, which included animals simultaneously infected by E. canis and B. vogeli and/or A. platys. The serum concentrations of the thyroid hormones were measured at two time points: before (D1) and after (D2) the 28-day treatment with generic doxycycline chlorohydrate (DC) at a dose of 10 mg/kg SID. On D2, another nPCR was carried out to check the efficacy of the treatment. On D2, in both groups, all dogs became negative for E. canis; however, 8 animals remained infected or were reinfected by other hemoparasites. On D1, 4 dogs in G1 exhibited low TT3 in conjunction with low TT4; one of the dogs had increased TT3 alone, and another dog had an increased TT3 accompanied by decreased TT4. In G2, on D1, one dog exhibited high TT3 accompanied by a decreased concentration of TT4; 2 dogs had decreased TT4; 2 dogs had increased TT3; and one dog had both TT3 and TT4 decreased. On D2, with only one exception, the animals in G1 that became negative for all hemoparasites under study exhibited normal serum levels of TT3 and TT4. Three dogs in G1, which were reinfected on D2, sustained decreased TT4 serum concentrations. Whereas, in G1 on D2, only one dog remained with a reduced serum TT4 concentration.
Discussion: DC was effective at eliminating infection by E. canis in all dogs on D2. Even though this drug was unable to prevent reinfection of the animals by other hemoparasites, and in spite of divergent results on its efficacy at eliminating babesiosis and anaplasmosis, a clinical improvement was observed in all patients. A decrease in the serum concentrations of thyroid hormones (ESS) may occur in dogs with severe non-thyroid related diseases. Different authors have demonstrated the presence of ESS in dogs with hemoparasitoses; however, this is the first study to provide evidence on the existence of this syndrome in dogs with hemoparasitoses in Brazil, including dogs simultaneously infected by E. canis and B. vogeli and/or A. platys.We observed a reduction in TT3 and/or TT4 in dogs infected by E. canis, B. vogeli, and A. platys. We believe these results may help assessment of prognosis and patient follow-up, as TT4 concentrations returned to normal levels in all dogs that became negative for all hemoparasites after treatment; and only one dog in G1 sustained increased TT3, albeit lower than observed on D1. In animals of G1 that were reinfected after treatment started, TT3 returned to normal, even though TT4 levels remained decreased. In sum, all dogs in G1 and G2 exhibited TT3 and/or TT4 concentrations outside of the reference value ranges on D1, which indicates that alterations in the levels of thyroid hormones were due to infection by the hemoparasites. The animals infected by E. canis alone or simultaneously infected by B. vogeli and/or A. platys exhibited ESS.
Bouzouraa T., René-Martellet M., Chêne J., Attipa C., Lebert I., Chalvet-Monfray K., Cadoré J.L., Halos L. & Chabanne L. 2016. Clinical and laboratory features of canine Anaplasma platys infection in 32 naturally infected dogs in the Mediterranean basin. Ticks and Tick-Borne Diseases. 7(6): 1256-1264. DOI: 10.1016/j.ttbdis.2016.07.004
Da Silveira J.A.G., Rabelo É.M.L. & Ribeiro M.F.B. 2011. Detection of Theileria and Babesia in brown brocket deer (Mazama gouazoubira) and marsh deer (Blastocerus dichotomus) in the State of Minas Gerais, Brazil. Veterinary Parasitology. 177(1-2): 61-66. DOI: 10.1016/j.vetpar.2010.10.044
Dantas-Torres F., Silva Y.Y., Miranda D.E.O., Sales K.G.S., Figueredo L.A. & Otranto D. 2018. Ehrlichia spp. infection in rural dogs from remote indigenous villages in north-eastern Brazil. Parasites and Vectors. 11(1): 139. DOI: 10.1186/s13071-018-2738-3
Elliott D.A., King L.G. & Zerbe C.A. 1995. Thyroid Hormone Concentrations In Critically III Canine Intensive Care Patients. Journal of Veterinary Emergency and Critical Care. 5(1): 17-23. DOI: 10.1111/j.1476-4431.1995.tb00023.x
Gaunt S.D., Beall M.J., Stillman B.A., Lorentzen L., Diniz P.P.V.P., Chandrashekar R. & Breitschwerdt E.B. 2010. Experimental infection and co-infection of dogs with Anaplasma platys and Ehrlichia canis: Hematologic, serologic and molecular findings. Parasites and Vectors. 3(1): 33. DOI: 10.1186/1756-3305-3-33
Hari Kumar K.V.S., Pawah A. & Manrai M. 2016. Occult endocrine dysfunction in patients with cirrhosis of liver. Journal of Family Medicine and Primary Care. 5(3): 576. DOI: 10.4103/2249-4863.197293
Harrus S., Waner T., Aizenberg I., Foley J.E., Poland A.M. & Bark H. 1998. Amplification of ehrlichial DNA from dogs 34 months after infection with Ehrlichia canis. Journal of Clinical Microbiology. 36(1): 73-76. http://www.ncbi.nlm.nih.gov/pubmed/9431923
Hennemann G. & Krenning E.P. 2007. The kinetics of thyroid hormone transporters and their role in non-thyroidal illness and starvation. Best Practice and Research in Clinical Endocrinology and Metabolism. 21(2): 323-338. DOI: 10.1016/j.beem.2007.03.007
Kumar A., Varshney J.P. & Varshney V.P. 2006. Endocrine dysfunction in chronic severe ehrlichiosis with or without babesiosis in dogs. Veterinary Research Communications. 30(8): 911-916. DOI: 10.1007/s11259-006-3403-4
Mooney C.T. 2011. Canine hypothyroidism: A review of aetiology and diagnosis Canine hypothyroidism: A review of aetiology and diagnosis. New Zealand Veterinary Journal. 59(3): 105-114. DOI: 10.1080/00480169.2011.563729
Mooney C.T., Shiel R.E. & Dixon R.M. 2008. Thyroid hormone abnormalities and outcome in dogs with non-thyroidal illness. Journal of Small Animal Practice. 49(1): 11-16. DOI: 10.1111/j.1748-5827.2007.00418.x
Neer T.M., Breitschwerdt E.B. Greene R.T. & Lappin M.R. 2002. Consensus statement on ehrlichial disease of small animals from the infectious disease study group of the ACVIM. American College of Veterinary Internal Medicine. Journal of Veterinary Internal Medicine. 16(3): 309-315. DOI: 10.1111/j.1939-1676.2002.tb02374.x
Niwetpathomwat A. 2006. A retrospective study of the therapeutic efficacy of doxycycline on concurrent canine ehrlichiosis and babesiosis in a veterinary hospital population. Comparative Clinical Pathology. 15(4): 215-219. DOI: 10.1007/s00580-006-0654-y
Passos L.M.F., Geiger S.M., Ribeiro M.F.B., Pfister K. & Zahler-Rinder M. 2005. First molecular detection of Babesia vogeli in dogs from Brazil. Veterinary Parasitology. 127(1): 81-85. DOI: 10.1016/j.vetpar.2004.07.028
Plikat K., Langgartner J., Buettner R., Bollheimer L.C., Woenckhaus U., Schölmerich J. & Wrede C.E. 2007. Frequency and outcome of patients with nonthyroidal illness syndrome in a medical intensive care unit. Metabolism: Clinical and Experimental. 56(2): 239-244. DOI: 10.1016/j.metabol.2006.09.020
Schoeman J.P., Rees P. & Herrtage M.E. 2007. Endocrine predictors of mortality in canine babesiosis caused by Babesia canis rossi. Veterinary Parasitology. 148(2): 75-82. DOI: 10.1016/j.vetpar.2007.06.010
Scott-Moncrieff J.C. 2007. Clinical Signs and Concurrent Diseases of Hypothyroidism in Dogs and Cats. Veterinary Clinics of North America - Small Animal Practice. 37(4): 709-722. DOI: 10.1016/j.cvsm.2007.03.003
Soares R., Ramos C.A., Pedroso T., Babo-Terra V., Cleveland H. & Araújo F. 2017. Molecular survey of Anaplasma platys and Ehrlichia canis in dogs from Campo grande, Mato Grosso do Sul, Brazil. Anais Da Academia Brasileira de Ciências. 89(1): 301-306. DOI: 10.1590/0001-3765201720150556
Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. 30(12): 2725-2729. DOI: 10.1093/molbev/mst197
Tosta C.E. 1983. Modificação da resposta imune por agentes quimioterápicos. Revista da Sociedade Brasileira de Medicina Tropical. 16(1): 3-5.
Vercammen F., De Deken R. & Maes L. 1996. Prophylactic treatment of experimental canine babesiosis (Babesia canis) with doxycycline. Veterinary Parasitology. 66(3-4): 251-255. DOI: 10.1016/s0304-4017(96)01016-3
Vieira R.F.C., Biondo A.W., Guimarães A.M.S., Santos A.P., Santos R.P., Dutra L.H., Diniz P.P.V.P., De Morais H.A., Messick J.B., Labruna M.B. & Vidotto O. 2011. Ehrlichiosis in Brazil. Revista Brasileira de Parasitologia Veterinária. 20(1): 1-12. DOI: 10.1590/s1984-29612011000100002
Villaescusa A., García-Sancho M., Rodríguez-Franco F., Tesouro M. & Sainz T. 2015. Effects of doxycycline on haematology, blood chemistry and peripheral blood lymphocyte subsets of healthy dogs and dogs naturally infected with Ehrlichia canis. Veterinary Journal. 204(3): 263-268. DOI: 10.1016/j.tvjl.2015.03.031
Wajner S.M. & Maia A.L. 2012. New Insights toward the Acute Non-Thyroidal Illness Syndrome. Frontiers in Endocrinology. 12(3): 1-7. DOI: 10.3389/fendo.2012.00008
Zygner W., Gójska-Zygner O., Baska P. & Długosz E. 2015. Low T3 syndrome in canine babesiosis associated with increased serum IL-6 concentration and azotaemia. Veterinary Parasitology. 211(1-2): 23-27. DOI: 10.1016/j.vetpar.2015.04.023
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