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The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves' Disease

Yıl 2025, Cilt: 12 Sayı: 1, 125 - 133, 26.03.2025
https://doi.org/10.34087/cbusbed.1593450

Öz

Abstract
Objective: Thyroid stimulating immunoglobulin (TSI) is used in the differential diagnosis of thyrotoxicosis and disease recurrence and activity. However, the accessibility and the cost can limit the use of TSI. In our study, we investigated the existence of easily accessible markers that can be used instead of TSI in the diagnosis and follow-up of Graves' disease (GD). The aim was to evaluate the relationship between TSI levels and inflammatory markers such as neutrophil-lymphocyte ratio (NLR), monocyte-lymphocyte ratio (MLR), platelet-lymphocyte ratio (TLR), systemic immune inflammation (SII) index, pan-immune inflammation value (PIV) obtained from the complete blood count of the patients at the beginning and 6 months after anti-thyroid treatment.
Materials and Methods: 162 patients diagnosed with Graves' disease were retrospectively investigated. According to the free T4 level, the patients were divided into 3 groups as mild, moderate, and severe disease. Thyroid function tests, hemogram parameters, and TSI values of the patients at the time of diagnosis and after 6 months of anti-thyroid treatment were compared. The correlation of the statistically significant parameters with TSI was studied separately for each group.

Results: While there was a significant increase in hemoglobin (p=0.009), leukocyte (p=0.001), neutrophil (p=0.002), lymphocyte (p=0.002), eosinophil (p=0.033), basophil (p=0.001) and TSH (p=0.001) levels after treatment compared to the baseline, there was a significant decrease in monocyte (p=0.003), platelet (p=0.010), TLR (p=0.001), MLR (p=0.001), freeT3 (p=0.001), freeT4 (p=0.001) levels. The correlation of these statistically significant parameters with TSI was observed. When the baseline and 6th month post-treatment values were investigated in all patients; a weak positive correlation was detected between TSI and monocytes and MLR, and a weak positive correlation was detected with freeT3. A weak positive correlation was detected between TSI and RDW and freeT3 in the severe disease group.

Conclusion: Although a reliable marker that can be used as an alternative to TSI in the follow-up of Graves' disease has not been available, monocyte level, MLR and RDW in patients with severe Graves’ disease may predict an activation in the follow-up of the disease.

Kaynakça

  • 1. Cindoğlu Ç, Güler M, Eren MA, Sabuncu T. Hipertiroidi Hastalarında Tedavi Öncesi ve Sonrası Trombosit/Lenfosit ve Nötrofil/Lenfosit Oranlarının Değerlendirilmesi. Harran Üniversitesi Tıp Fakültesi Dergisi. 2020 Apr 29;
  • 2. Gardner DG, Shoback D. Greenspan Basic&Clinical Endocrinology.; 2019. Greenspan Temel ve Klinik Endokrinoloji . 2019;
  • 3. Türkiye Endokrinoloji ve Metabolizma Derneği Tiroid Hastalıkları Tanı ve Tedavi Kılavuzu. Ankara ; 2020. 55 p. 4. Dasgupta R, Atri A, Jebasingh F, Hepzhibah J, Christudoss P, Asha H, et al. Platelet-Lymphocyte Ratio as a Novel Surrogate Marker to Differentiate Thyrotoxic Patients with Graves Disease from Subacute Thyroiditis: a Cross-Sectional Study from South India. Endocrine Practice. 2020 Sep;26(9):939–44.
  • 5. Zhong JH, Huang DH, Chen ZY. Prognostic role of systemic immune-inflammation index in solid tumors: a systematic review and meta-analysis. Oncotarget. 2017 Sep 26;8(43):75381–8.
  • 6. Balas Ş, Çınkıl NC, Apaydın M. Şiddetli pankreatiti öngörmede yeni biyobelirteç; Sistemik immün-inflamasyon indeksi. Turkish Journal of Clinics and Laboratory. 2023 Sep 30;14(3):464–9.
  • 7. Stan MN, Durski JM, Brito JP, Bhagra S, Thapa P, Bahn RS. Cohort Study on Radioactive Iodine–Induced Hypothyroidism: Implications for Graves’ Ophthalmopathy and Optimal Timing for Thyroid Hormone Assessment. Thyroid. 2013 May;23(5):620–5.
  • 8. Murat B, Murat S, Ozgeyik M, Bilgin M. Comparison of pan‐immune‐inflammation value with other inflammation markers of long‐term survival after <scp>ST</scp> ‐segment elevation myocardial infarction. Eur J Clin Invest. 2023 Jan 20;53(1).
  • 9. Ross DS, Burch HB, Cooper DS, Greenlee MC, Laurberg P, Maia AL, et al. 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis. Thyroid. 2016 Oct;26(10):1343–421.
  • 10. Shaw B, Mehta AB. Pancytopenia responding to treatment of hyperthyroidism: a clinical case and review of the literature. Clin Lab Haematol. 2002 Dec;24(6):385–7.
  • 11. Aggarwal N, Tee SA, Saqib W, Fretwell T, Summerfield GP, Razvi S. Treatment of hyperthyroidism with antithyroid drugs corrects mild neutropenia in <scp>G</scp> raves’ disease. Clin Endocrinol (Oxf). 2016 Dec 21;85(6):949–53.
  • 12. Dağdeviren M, Akkan T, Yapar D, Karakaya S, Dağdeviren T, Ertuğrul D, et al. Can Neutrophil/Lymphocyte Ratio Be Used as an Indicator of Inflammation in Patients with Hyperthyroidism? J Med Biochem. 2019 Jan 1;0(0).
  • 13. Grymuła K, Paczkowska E, Dziedziejko V, Baśkiewicz-Masiuk M, Kawa M, Baumert B, et al. The influence of 3,3’,5-triiodo-l-thyronine on human haematopoiesis. Cell Prolif. 2007 Jun;40(3):302–15.
  • 14. Neutrophil to lymphocyte ratio, Monocyte to lymphocyte ratio, platelet to lymphocyte ratio in different etiological causes of thyrotoxicosis. Turk J Med Sci. 2019;
  • 15. Peng Y, Qi Y, Huang F, Chen X, Zhou Y, Ye L, et al. Down-regulated resistin level in consequence of decreased neutrophil counts in untreated Grave’s disease. Oncotarget. 2016 Nov 29;7(48):78680–7.
  • 16. Turan E. Evaluation of neutrophil-to-lymphocyte ratio and hematologic parameters in patients with Graves’ disease. Bratislava Medical Journal. 2019;120(06):476–80.
  • 17. Gokce A, Omma T, Çelikc M, Taşkaldıran I. An overview of the hematological picture with antithyroid therapy in Graves’ disease. Acta Facultatis Medicae Naissensis. 2022;39(4):467–75.
  • 18. Yuri Gasparyan A, Ayvazyan L, P. Mikhailidis D, D. Kitas G. Mean Platelet Volume: A Link Between Thrombosis and Inflammation? Curr Pharm Des. 2011 Jan 1;17(1):47–58.
  • 19. Lippi G, Danese E, Montagnana M, Nouvenne A, Meschi T, Borghi L. Mean platelet volume is significantly associated with serum levels of thyroid-stimulating hormone in a cohort of older euthyroid subjects. Endocr Res. 2015 Oct 2;40(4):227–30.
  • 20. Cao Y tian, Zhang K yu, Sun J, Lou Y, Lv T su, Yang X, et al. Platelet abnormalities in autoimmune thyroid diseases: A systematic review and meta-analysis. Front Immunol. 2022 Dec 22;13.
  • 21. Shi L, Qin X, Wang H, Xia Y, Li Y, Chen X, et al. Elevated neutrophil-to-lymphocyte ratio and monocyte-to-lymphocyte ratio and decreased platelet-to-lymphocyte ratio are associated with poor prognosis in multiple myeloma. Oncotarget. 2017 Mar 21;8(12):18792–801.
  • 22. Li J, Jiang R, Liu WS, Liu Q, Xu M, Feng QS, et al. A Large Cohort Study Reveals the Association of Elevated Peripheral Blood Lymphocyte-to-Monocyte Ratio with Favorable Prognosis in Nasopharyngeal Carcinoma. PLoS One. 2013 Dec 27;8(12):e83069.
  • 23. Artemniak-Wojtowicz D, Witkowska-Sędek E, Borowiec A, Pyrżak B. Peripheral blood picture and aminotransferase activity in children with newly diagnosed Graves’ disease at baseline and after the initiation of antithyroid drug therapy. Central European Journal of Immunology. 2019;44(2):132–7.
  • 24. Bozkurt E, Beysel S, Hafızoğlu M, Koca OH, Vurmaz A, Gökaslan S. Graves Hastalarında Kardiyovasküler Risk Faktörü Olarak: MPV VE RDW. Kocatepe Tıp Dergisi. 2020 Jul 1;21(3):251–7.
  • 25. Ozbek E, Besiroglu H, Ozer K, Horsanali MO, Gorgel SN. Systemic immune inflammation index is a promising non-invasive marker for the prognosis of the patients with localized renal cell carcinoma. Int Urol Nephrol. 2020 Aug 14;52(8):1455–63.
  • 26. Şahin AB, Cubukcu E, Ocak B, Deligonul A, Oyucu Orhan S, Tolunay S, et al. Low pan-immune-inflammation-value predicts better chemotherapy response and survival in breast cancer patients treated with neoadjuvant chemotherapy. Sci Rep. 2021 Jul 19;11(1):14662.

Graves Hastalığında Başlangıç ve Tedavinin 6. Ayında Hemogramdaki İnflamatuar Parametreler ile Tiroid Stimulan İmmunglobulin (TSI) Düzeyi Arasındaki İlişki

Yıl 2025, Cilt: 12 Sayı: 1, 125 - 133, 26.03.2025
https://doi.org/10.34087/cbusbed.1593450

Öz

Öz
Giriş ve Amaç: Tirotoksikozun ayırıcı tanısında, hastalık nüksü ve aktivitesini göstermede TSI kullanılmaktadır. Ancak ulaşılabilirlik ve maliyet TSI kullanımını sınırlandırmaktadır. Çalışmamızda, Graves hastalığı (GH) tanı ve takibinde TSI yerine kullanılabilecek ve kolay ulaşılabilen belirteç varlığı araştırılmıştır. Hastaların başlangıç ve antitiroidal tedavi sonrası 6. aydaki tam kan sayımından elde edilen nötrofil lenfosit oranı (NLO), monosit lenfosit oranının (MLO), trombosit lenfosit oranı (TLO), sistemik immün inflamasyon (SII) indeksi, pan-immün inflamasyon değeri (PIV) gibi inflamatuar belirteçler ile TSI düzeyleri arasındaki ilişkinin değerlendirmesi amaçlanmıştır.
Gereç ve Yöntemler: Graves hastalığı tanılı 162 hasta retrospektif olarak incelendi. Serbest T4 düzeyine göre hastalar, hafif, orta, ağır şiddetli hastalık olarak 3’e ayrıldı. Hastaların tanı anındaki ve 6 ay antitiroid tedavi sonrasındaki tiroid fonksiyon testleri, hemogram parametreleri ve TSI değerleri karşılaştırıldı. İstatistiksel olarak anlamlı bulunan parametrelerin TSI ile korelasyonu her grup için ayrı ayrı incelendi.
Bulgular: Tedavi sonrası başlangıca göre hemoglobin (p=0.009), lökosit (p=0.001), nötrofil (p=0.002), lenfosit (p=0.002), eozinofil (p=0.033), bazofil (p=0.001) ve TSH (p=0.001) anlamlı artış varken; monosit (p=0.003), trombosit (p=0.010), TLO (p=0.001), MLO (p=0.001), sT3 (p=0.001), sT4 (p=0.001) düzeylerinde anlamlı azalma izlendi. İstatistiksel olarak anlamlı bulunan bu parametrelerin TSI ile korelasyonu incelendi. Tüm hastalarda başlangıç ve tedavi sonrası 6. ay değerleri incelendiğinde; TSI ile monosit ve MLO arasında pozitif yönde çok zayıf korelasyon ve sT3 ile pozitif yönde zayıf korelasyon tespit edildi. Ağır şiddetli hastalık grubunda TSI ile RDW ve sT3 arasında pozitif yönde zayıf korelasyon saptandı.
Sonuç: Graves hastalığı takibinde TSI’ya alternatif olarak kullanılabilecek güvenilir bir belirteç saptanmamış olsa da monosit, MLO ve ağır şiddetli hastalarda RDW’nin hastalık takibinde aktivasyonu göstermede fikir verebileceği düşünülebilir.

Kaynakça

  • 1. Cindoğlu Ç, Güler M, Eren MA, Sabuncu T. Hipertiroidi Hastalarında Tedavi Öncesi ve Sonrası Trombosit/Lenfosit ve Nötrofil/Lenfosit Oranlarının Değerlendirilmesi. Harran Üniversitesi Tıp Fakültesi Dergisi. 2020 Apr 29;
  • 2. Gardner DG, Shoback D. Greenspan Basic&Clinical Endocrinology.; 2019. Greenspan Temel ve Klinik Endokrinoloji . 2019;
  • 3. Türkiye Endokrinoloji ve Metabolizma Derneği Tiroid Hastalıkları Tanı ve Tedavi Kılavuzu. Ankara ; 2020. 55 p. 4. Dasgupta R, Atri A, Jebasingh F, Hepzhibah J, Christudoss P, Asha H, et al. Platelet-Lymphocyte Ratio as a Novel Surrogate Marker to Differentiate Thyrotoxic Patients with Graves Disease from Subacute Thyroiditis: a Cross-Sectional Study from South India. Endocrine Practice. 2020 Sep;26(9):939–44.
  • 5. Zhong JH, Huang DH, Chen ZY. Prognostic role of systemic immune-inflammation index in solid tumors: a systematic review and meta-analysis. Oncotarget. 2017 Sep 26;8(43):75381–8.
  • 6. Balas Ş, Çınkıl NC, Apaydın M. Şiddetli pankreatiti öngörmede yeni biyobelirteç; Sistemik immün-inflamasyon indeksi. Turkish Journal of Clinics and Laboratory. 2023 Sep 30;14(3):464–9.
  • 7. Stan MN, Durski JM, Brito JP, Bhagra S, Thapa P, Bahn RS. Cohort Study on Radioactive Iodine–Induced Hypothyroidism: Implications for Graves’ Ophthalmopathy and Optimal Timing for Thyroid Hormone Assessment. Thyroid. 2013 May;23(5):620–5.
  • 8. Murat B, Murat S, Ozgeyik M, Bilgin M. Comparison of pan‐immune‐inflammation value with other inflammation markers of long‐term survival after <scp>ST</scp> ‐segment elevation myocardial infarction. Eur J Clin Invest. 2023 Jan 20;53(1).
  • 9. Ross DS, Burch HB, Cooper DS, Greenlee MC, Laurberg P, Maia AL, et al. 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis. Thyroid. 2016 Oct;26(10):1343–421.
  • 10. Shaw B, Mehta AB. Pancytopenia responding to treatment of hyperthyroidism: a clinical case and review of the literature. Clin Lab Haematol. 2002 Dec;24(6):385–7.
  • 11. Aggarwal N, Tee SA, Saqib W, Fretwell T, Summerfield GP, Razvi S. Treatment of hyperthyroidism with antithyroid drugs corrects mild neutropenia in <scp>G</scp> raves’ disease. Clin Endocrinol (Oxf). 2016 Dec 21;85(6):949–53.
  • 12. Dağdeviren M, Akkan T, Yapar D, Karakaya S, Dağdeviren T, Ertuğrul D, et al. Can Neutrophil/Lymphocyte Ratio Be Used as an Indicator of Inflammation in Patients with Hyperthyroidism? J Med Biochem. 2019 Jan 1;0(0).
  • 13. Grymuła K, Paczkowska E, Dziedziejko V, Baśkiewicz-Masiuk M, Kawa M, Baumert B, et al. The influence of 3,3’,5-triiodo-l-thyronine on human haematopoiesis. Cell Prolif. 2007 Jun;40(3):302–15.
  • 14. Neutrophil to lymphocyte ratio, Monocyte to lymphocyte ratio, platelet to lymphocyte ratio in different etiological causes of thyrotoxicosis. Turk J Med Sci. 2019;
  • 15. Peng Y, Qi Y, Huang F, Chen X, Zhou Y, Ye L, et al. Down-regulated resistin level in consequence of decreased neutrophil counts in untreated Grave’s disease. Oncotarget. 2016 Nov 29;7(48):78680–7.
  • 16. Turan E. Evaluation of neutrophil-to-lymphocyte ratio and hematologic parameters in patients with Graves’ disease. Bratislava Medical Journal. 2019;120(06):476–80.
  • 17. Gokce A, Omma T, Çelikc M, Taşkaldıran I. An overview of the hematological picture with antithyroid therapy in Graves’ disease. Acta Facultatis Medicae Naissensis. 2022;39(4):467–75.
  • 18. Yuri Gasparyan A, Ayvazyan L, P. Mikhailidis D, D. Kitas G. Mean Platelet Volume: A Link Between Thrombosis and Inflammation? Curr Pharm Des. 2011 Jan 1;17(1):47–58.
  • 19. Lippi G, Danese E, Montagnana M, Nouvenne A, Meschi T, Borghi L. Mean platelet volume is significantly associated with serum levels of thyroid-stimulating hormone in a cohort of older euthyroid subjects. Endocr Res. 2015 Oct 2;40(4):227–30.
  • 20. Cao Y tian, Zhang K yu, Sun J, Lou Y, Lv T su, Yang X, et al. Platelet abnormalities in autoimmune thyroid diseases: A systematic review and meta-analysis. Front Immunol. 2022 Dec 22;13.
  • 21. Shi L, Qin X, Wang H, Xia Y, Li Y, Chen X, et al. Elevated neutrophil-to-lymphocyte ratio and monocyte-to-lymphocyte ratio and decreased platelet-to-lymphocyte ratio are associated with poor prognosis in multiple myeloma. Oncotarget. 2017 Mar 21;8(12):18792–801.
  • 22. Li J, Jiang R, Liu WS, Liu Q, Xu M, Feng QS, et al. A Large Cohort Study Reveals the Association of Elevated Peripheral Blood Lymphocyte-to-Monocyte Ratio with Favorable Prognosis in Nasopharyngeal Carcinoma. PLoS One. 2013 Dec 27;8(12):e83069.
  • 23. Artemniak-Wojtowicz D, Witkowska-Sędek E, Borowiec A, Pyrżak B. Peripheral blood picture and aminotransferase activity in children with newly diagnosed Graves’ disease at baseline and after the initiation of antithyroid drug therapy. Central European Journal of Immunology. 2019;44(2):132–7.
  • 24. Bozkurt E, Beysel S, Hafızoğlu M, Koca OH, Vurmaz A, Gökaslan S. Graves Hastalarında Kardiyovasküler Risk Faktörü Olarak: MPV VE RDW. Kocatepe Tıp Dergisi. 2020 Jul 1;21(3):251–7.
  • 25. Ozbek E, Besiroglu H, Ozer K, Horsanali MO, Gorgel SN. Systemic immune inflammation index is a promising non-invasive marker for the prognosis of the patients with localized renal cell carcinoma. Int Urol Nephrol. 2020 Aug 14;52(8):1455–63.
  • 26. Şahin AB, Cubukcu E, Ocak B, Deligonul A, Oyucu Orhan S, Tolunay S, et al. Low pan-immune-inflammation-value predicts better chemotherapy response and survival in breast cancer patients treated with neoadjuvant chemotherapy. Sci Rep. 2021 Jul 19;11(1):14662.
Toplam 25 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Endokrinoloji
Bölüm Araştırma Makalesi
Yazarlar

Sümeyye Gökduman 0009-0005-3524-4237

Nilüfer Özdemir 0000-0002-0719-988X

Mine Miskioğlu 0000-0003-2416-7991

Can Akçura 0000-0003-4182-9002

Berna Bilgin Şahin 0000-0003-2509-3330

Zeliha Hekimsoy 0000-0002-6003-0485

Erken Görünüm Tarihi 26 Mart 2025
Yayımlanma Tarihi 26 Mart 2025
Gönderilme Tarihi 29 Kasım 2024
Kabul Tarihi 24 Şubat 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 12 Sayı: 1

Kaynak Göster

APA Gökduman, S., Özdemir, N., Miskioğlu, M., Akçura, C., vd. (2025). The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease. Celal Bayar Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi, 12(1), 125-133. https://doi.org/10.34087/cbusbed.1593450
AMA Gökduman S, Özdemir N, Miskioğlu M, Akçura C, Bilgin Şahin B, Hekimsoy Z. The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease. CBU-SBED. Mart 2025;12(1):125-133. doi:10.34087/cbusbed.1593450
Chicago Gökduman, Sümeyye, Nilüfer Özdemir, Mine Miskioğlu, Can Akçura, Berna Bilgin Şahin, ve Zeliha Hekimsoy. “The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease”. Celal Bayar Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi 12, sy. 1 (Mart 2025): 125-33. https://doi.org/10.34087/cbusbed.1593450.
EndNote Gökduman S, Özdemir N, Miskioğlu M, Akçura C, Bilgin Şahin B, Hekimsoy Z (01 Mart 2025) The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease. Celal Bayar Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi 12 1 125–133.
IEEE S. Gökduman, N. Özdemir, M. Miskioğlu, C. Akçura, B. Bilgin Şahin, ve Z. Hekimsoy, “The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease”, CBU-SBED, c. 12, sy. 1, ss. 125–133, 2025, doi: 10.34087/cbusbed.1593450.
ISNAD Gökduman, Sümeyye vd. “The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease”. Celal Bayar Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi 12/1 (Mart 2025), 125-133. https://doi.org/10.34087/cbusbed.1593450.
JAMA Gökduman S, Özdemir N, Miskioğlu M, Akçura C, Bilgin Şahin B, Hekimsoy Z. The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease. CBU-SBED. 2025;12:125–133.
MLA Gökduman, Sümeyye vd. “The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease”. Celal Bayar Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi, c. 12, sy. 1, 2025, ss. 125-33, doi:10.34087/cbusbed.1593450.
Vancouver Gökduman S, Özdemir N, Miskioğlu M, Akçura C, Bilgin Şahin B, Hekimsoy Z. The Relationship Between Inflammatory Parameters in Hemogram and Thyroid Stimulating Immunoglobulin (TSI) Levels at the Beginning and the 6th Month of Treatment in Graves’ Disease. CBU-SBED. 2025;12(1):125-33.