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Association between inflammatory markers and primary hyperparathyroidism

Year 2019, , 241 - 247, 26.10.2019
https://doi.org/10.30565/medalanya.568224

Abstract

Aim: Primary hyperparathyroidism (PHP) is associated with systemic inflam-mation. The effect of parathyroidectomy (PTX) on inflammatory markers is contro-versial. The aim of our study was to investigate changes in inflammatory markers including C-reactive protein (hs-CRP), platelet-to-lymphocyte ratio (PLR), and red cell distribution width (RDW) before and after PTX. 

Patients and Methods: PHP patients (n=55) and age and sex matched healthy controls (n=50) were included in the study. The clinical and laboratory results of the PHP and control groups were compared before PTX and 6-months after PTX.

Results: At baseline, serum hs-CRP (4.01±3.44 vs. 2.48±1.73 mg/L), PLR (127.21±25.77 vs. 103.63±32.52), RDW (15.50±2.53 % vs. 13.49±0.70 %) values were higher in the PHP group than in the control group (p<0.05). After PTX, hs-CRP (3.59±3.07 mg/L), PLR (123.03±31.94), RDW (14.25±1.51 %) values did not change (p>0.05). Post-PTX hs-CRP, PLR, and RDW values were higher in the PHP group than in the control group (p<0.05). PTH value was positively correlated with pre-PTX hs-CRP (r2=0.377, p=0.001), PLR (r2=0.234, p=0.023), RDW (r2=0.296, p=0.004).

Conclusion: Before PTX, inflammatory markers were higher in PHP patients com-pared with healthy controls. After PTX, the inflammatory markers did not significantly decrease; however these postoperative markers were higher than controls. İnflam-mation occurs in PHP patients, and also shows a partial recovery from inflammation despite successful surgery. 

References

  • 1. Cheng, S.-P., Liu, C.-L., Liu, T.-P., Hsu, Y.-C., and Lee, J.-J. Association between Parathyroid Hormone Levels and Inflammatory Markers among US Adults. Mediators Inflamm. 2014;1–8. DOI: 10.1155/2014/709024
  • 2. Beysel, S., Caliskan, M., Kizilgul, M., Apaydin, M., Kan, S., Ozbek, M et al. Parathyroidectomy improves cardiovascular risk factors in normocalcemic and hypercalcemic primary hyperparathyroidism. BMC Cardiovasc. Disord. 2019;19(1):106. DOI: 10.1186/s12872-019-1093-4
  • 3. Haglund, F., Hallström, B.M., Nilsson, I.-L., Höög, A., Juhlin, C.C., and Larsson, C. Inflammatory infiltrates in parathyroid tumors. Eur. J. Endocrinol. 2017;177(6):445–53. DOI: 10.1530/EJE-17-0277
  • 4. Yang, P.-S., Liu, C.-L., Liu, T.-P., Chen, H.-H., Wu, C.-J., and Cheng, S.-P. Parathyroidectomy decreases neutrophil-to-lymphocyte and platelet-to-lymphocyte ratios. J. Surg. Res. 2018;224:169–175. DOI: 10.1016/j.jss.2017.12.016
  • 5. Christensen, M.H.E., Fenne, I.S., Nordbø, Y., Varhaug, J.E., Nygård, K.O., Lien, E.A et al. Novel inflammatory biomarkers in primary hyperparathyroidism. Eur. J. Endocrinol 2015;173(1):9–17. DOI: 10.1530/EJE-14-1038
  • 6. Ogard, C.G., Engelmann, M.D., Kistorp, C., Nielsen, S.L., and Vestergaard, H. Increased plasma N-terminal pro-B-type natriuretic peptide and markers of inflammation related to atherosclerosis in patients with primary hyperparathyroidism. Clin. Endocrinol. (Oxf.) 2005;63(5):493–8. DOI: 10.1111/j.1365-2265.2005.02363.x
  • 7. Bollerslev, J., Rosen, T., Mollerup, C.L., Nordenström, J., Baranowski, M., Franco, C et al. Effect of surgery on cardiovascular risk factors in mild primary hyperparathyroidism. J. Clin. Endocrinol. Metab. 2009;94(7):2255–61. DOI: 10.1210/jc.2008-2742
  • 8. Guo, C.Y., Holland, P.A., Jackson, B.F., Hannon, R.A., Rogers, A., Harrison, B.J et al. Immediate changes in biochemical markers of bone turnover and circulating interleukin-6 after parathyroidectomy for primary hyperparathyroidism. Eur. J. Endocrinol. 200;142(5):451–9. ISSN: 0804-4643
  • 9. Emam, A.A., Mousa, S.G., Ahmed, K.Y., and Al-Azab, A.A. Inflammatory biomarkers in patients with asymptomatic primary hyperparathyroidism. Med. Princ. Pract. Int. J. Kuwait Univ. Health Sci. Cent. 2012;21(3):249–53. DOI: 10.1159/000334588
  • 10. Li, N., Zhou, H., and Tang, Q. Red Blood Cell Distribution Width: A Novel Predictive Indicator for Cardiovascular and Cerebrovascular Diseases. Dis. Markers 2017, 1–23. DOI: 10.1155/2017/7089493
  • 11. Kurtul, A., and Ornek, E. Platelet to Lymphocyte Ratio in Cardiovascular Diseases: A Systematic Review. Angiology 2019. 000331971984518. DOI: 10.1177/0003319719845186
  • 12. Çalış H, Arıcı AG, Doğru V, Arıcı C. Measurement of Parathyroid Hormone Level in Early Diagnosis of Hypocalcemia After Total Thyroidectomy. Acta Med. Alanya 2019; 3(1):21-26. DOI:10.30565/medalanya.384037
  • 13. Almqvist, E.G., Bondeson, A.-G., Bondeson, L., and Svensson, J. Increased markers of inflammation and endothelial dysfunction in patients with mild primary hyperparathyroidism. Scand. J. Clin. Lab. Invest. 2011;71(2):139–44.
  • 14. Christensen, M.H.E., Pedersen, E.K.R., Nordbø, Y., Varhaug, J.E., Midttun, Ø., Ueland, P.M et al. Vitamin B6 status and interferon-γ-mediated immune activation in primary hyperparathyroidism. J. Intern. Med. 2012;272(6):583–91. DOI: 10.1111/j.1365-2796.2012.02570.x
  • 15. Kritchevsky, S.B., Tooze, J.A., Neiberg, R.H., Schwartz, G.G., Hausman, D.B., Johnson, M.A et al. 25-Hydroxyvitamin D, parathyroid hormone, and mortality in black and white older adults: the health ABC study. J. Clin. Endocrinol. Metab. 2012;97(11):4156–65. DOI: 10.1210/jc.2012-1551
  • 16. Aydin, O., and Pehlivanli, F. Paratiroid Adenomunun Ameliyat Öncesi Tanısında Öngörücü Bir Biyobelirteç Olarak Trombosit/Lenfosit Oranı. Kırıkkale Üniversitesi Tıp Fakültesi Derg. 2019:73–79. DOI: 10.24938/kutfd.522955
  • 17. Li, W., Liu, Q., and Tang, Y. Platelet to lymphocyte ratio in the prediction of adverse outcomes after acute coronary syndrome: a meta-analysis. Sci. Rep. 2017;7(1):40426. DOI: 10.1038/srep40426
  • 18. Lippi, G., Targher, G., Montagnana, M., Salvagno, G.L., Zoppini, G., and Guidi, G.C. Relation between red blood cell distribution width and inflammatory biomarkers in a large cohort of unselected outpatients. Arch. Pathol. Lab. Med. 2009;133(4):628–32. DOI: 10.1043/1543-2165-133.4.628
  • 19. Christensen, M.H.E., Dankel, S.N., Nordbø, Y., Varhaug, J.E., Almås, B., Lien, E.A et al. Primary hyperparathyroidism influences the expression of inflammatory and metabolic genes in adipose tissue. PloS One 2011;6(6):e20481. PMID: 21698093
  • 20. Wu, C.-C., Chang, J.-H., Chen, C.-C., Su, S.-B., Yang, L.-K., Ma, W.-Y et al. Calcitriol treatment attenuates inflammation and oxidative stress in hemodialysis patients with secondary hyperparathyroidism. Tohoku J. Exp. Med. 2011;223(3):153–9. PMID: 21350317
  • 21. Zeren, S., Yaylak, F., Ozbay, I., and Bayhan, Z. Relationship Between the Neutrophil to Lymphocyte Ratio and Parathyroid Adenoma Size in Patients With Primary Hyperparathyroidism. Int. Surg. 100, 2015;100(7-8):1185–9. DOI: 10.9738/INTSURG-D-15-00044.1
  • 22. Ahbap, E., Sakaci, T., Kara, E., Sahutoglu, T., Koc, Y., Basturk, T et al. Neutrophil-to-lymphocyte ratio and platelet-tolymphocyte ratio in evaluation of inflammation in end-stage renal disease. Clin. Nephrol.2016; 85(4):199–208. DOI: 10.5414/CN108584
  • 23. Zhang, Q., Cao, X., Zhou, J., Ding, R., Huang, J., Cai, G et al. Red cell distribution width reflects the early stage residual renal function in peritoneal dialysis patients. Saudi J. Kidney Dis. Transplant. Off. Publ. Saudi Cent. Organ Transplant. Saudi Arab. 2018;29(5):1082–91. DOI: 10.4103/1319-2442.243950
  • 24. Perlstein, T.S., Weuve, J., Pfeffer, M.A., and Beckman, J.A. Red Blood Cell Distribution Width and Mortality Risk in a Community-Based Prospective Cohort. Arch. Intern. Med. 2009;169(6):588. DOI: 10.1001/archinternmed.2009.55
  • 25. Ayça, B., Akin, F., Çelik, Ö., Yüksel, Y., Öztürk, D., Tekiner, F et al. Platelet to lymphocyte ratio as a prognostic marker in primary percutaneous coronary intervention. Platelets 2015;26(7):638–44. DOI: 10.3109/09537104.2014.968117

Inflamatuar belirteçler ve primer hiperparatiroidi arasındaki ilişki

Year 2019, , 241 - 247, 26.10.2019
https://doi.org/10.30565/medalanya.568224

Abstract

Amaç: Primer hiperparatiroidizm (PHP) sistemik inflamasyonla ilişkilidir. Paratiroidek-tominin (PTX) inflamatuar belirteçler üzerindeki etkisi tartışmalıdır. Çalışmamızın amacı, PTX öncesi ve sonrası C-reaktif protein (hs-CRP), trombosit / lenfosit oranı (TLO) ve kırmızı hücre dağılım genişliğini (RDW) içeren inflamatuar belirteçlerdeki değişiklikleri araştırmaktı.

Hastalar ve Yöntem: Çalışmaya PHP hastaları (n=55) ve yaş ve cinsiyet eşleştirilmiş sağlıklı kontroller (n=50) dahil edildi. PHP ve kontrol gruplarının klinik ve laboratuar sonuçları PTX'den önce ve PTX’den 6 ay sonra karşılaştırıldı.

Bulgular: Başlangıçta, serum hs-CRP (4,01±3,44’e karşın 2,48±1,73 mg/L), TLO (127,21±25,77’e karşın 103,63±32,52), RDW (15,50±2,53’e karşın 13,49±0,70 %) değerleri PHP grubunda, kontrol grubundan daha yüksekti (p<0,05). PTX’ten son-ra, hs-CRP (3,59±3,07 mg/L), TLO (123,03±31,94), RDW (14,25±1,51 %) değerleri değişmedi (p>0,05). PTX sonrası hs-CRP, TLO ve RDW değerleri PHP grubun-da, kontrol grubundan daha yüksekti (p<0,05). PTH değeri, PTX öncesi hs-CRP (r2=0,377, p=0,001), TLO (r2=0,234, p=0,023), RDW (r2=0,296, p=0,004) ile pozitif olarak korele idi.

Sonuç: PTX’den önce, PHP hastalarında inflamatuar belirteçler sağlıklı kontrollere kıyasla daha yüksekti. PTX'ten sonra, inflamatuar belirteçler istatiksel anlamlı azal-madı; ancak bu ameliyat sonrası belirteçler kontrollerden daha yüksekti. İnflamasyon PHP hastalarında görülür ve aynı zamanda başarılı bir ameliyat olmasına rağmen inflamasyondan kısmen iyileşme gösterir. 

References

  • 1. Cheng, S.-P., Liu, C.-L., Liu, T.-P., Hsu, Y.-C., and Lee, J.-J. Association between Parathyroid Hormone Levels and Inflammatory Markers among US Adults. Mediators Inflamm. 2014;1–8. DOI: 10.1155/2014/709024
  • 2. Beysel, S., Caliskan, M., Kizilgul, M., Apaydin, M., Kan, S., Ozbek, M et al. Parathyroidectomy improves cardiovascular risk factors in normocalcemic and hypercalcemic primary hyperparathyroidism. BMC Cardiovasc. Disord. 2019;19(1):106. DOI: 10.1186/s12872-019-1093-4
  • 3. Haglund, F., Hallström, B.M., Nilsson, I.-L., Höög, A., Juhlin, C.C., and Larsson, C. Inflammatory infiltrates in parathyroid tumors. Eur. J. Endocrinol. 2017;177(6):445–53. DOI: 10.1530/EJE-17-0277
  • 4. Yang, P.-S., Liu, C.-L., Liu, T.-P., Chen, H.-H., Wu, C.-J., and Cheng, S.-P. Parathyroidectomy decreases neutrophil-to-lymphocyte and platelet-to-lymphocyte ratios. J. Surg. Res. 2018;224:169–175. DOI: 10.1016/j.jss.2017.12.016
  • 5. Christensen, M.H.E., Fenne, I.S., Nordbø, Y., Varhaug, J.E., Nygård, K.O., Lien, E.A et al. Novel inflammatory biomarkers in primary hyperparathyroidism. Eur. J. Endocrinol 2015;173(1):9–17. DOI: 10.1530/EJE-14-1038
  • 6. Ogard, C.G., Engelmann, M.D., Kistorp, C., Nielsen, S.L., and Vestergaard, H. Increased plasma N-terminal pro-B-type natriuretic peptide and markers of inflammation related to atherosclerosis in patients with primary hyperparathyroidism. Clin. Endocrinol. (Oxf.) 2005;63(5):493–8. DOI: 10.1111/j.1365-2265.2005.02363.x
  • 7. Bollerslev, J., Rosen, T., Mollerup, C.L., Nordenström, J., Baranowski, M., Franco, C et al. Effect of surgery on cardiovascular risk factors in mild primary hyperparathyroidism. J. Clin. Endocrinol. Metab. 2009;94(7):2255–61. DOI: 10.1210/jc.2008-2742
  • 8. Guo, C.Y., Holland, P.A., Jackson, B.F., Hannon, R.A., Rogers, A., Harrison, B.J et al. Immediate changes in biochemical markers of bone turnover and circulating interleukin-6 after parathyroidectomy for primary hyperparathyroidism. Eur. J. Endocrinol. 200;142(5):451–9. ISSN: 0804-4643
  • 9. Emam, A.A., Mousa, S.G., Ahmed, K.Y., and Al-Azab, A.A. Inflammatory biomarkers in patients with asymptomatic primary hyperparathyroidism. Med. Princ. Pract. Int. J. Kuwait Univ. Health Sci. Cent. 2012;21(3):249–53. DOI: 10.1159/000334588
  • 10. Li, N., Zhou, H., and Tang, Q. Red Blood Cell Distribution Width: A Novel Predictive Indicator for Cardiovascular and Cerebrovascular Diseases. Dis. Markers 2017, 1–23. DOI: 10.1155/2017/7089493
  • 11. Kurtul, A., and Ornek, E. Platelet to Lymphocyte Ratio in Cardiovascular Diseases: A Systematic Review. Angiology 2019. 000331971984518. DOI: 10.1177/0003319719845186
  • 12. Çalış H, Arıcı AG, Doğru V, Arıcı C. Measurement of Parathyroid Hormone Level in Early Diagnosis of Hypocalcemia After Total Thyroidectomy. Acta Med. Alanya 2019; 3(1):21-26. DOI:10.30565/medalanya.384037
  • 13. Almqvist, E.G., Bondeson, A.-G., Bondeson, L., and Svensson, J. Increased markers of inflammation and endothelial dysfunction in patients with mild primary hyperparathyroidism. Scand. J. Clin. Lab. Invest. 2011;71(2):139–44.
  • 14. Christensen, M.H.E., Pedersen, E.K.R., Nordbø, Y., Varhaug, J.E., Midttun, Ø., Ueland, P.M et al. Vitamin B6 status and interferon-γ-mediated immune activation in primary hyperparathyroidism. J. Intern. Med. 2012;272(6):583–91. DOI: 10.1111/j.1365-2796.2012.02570.x
  • 15. Kritchevsky, S.B., Tooze, J.A., Neiberg, R.H., Schwartz, G.G., Hausman, D.B., Johnson, M.A et al. 25-Hydroxyvitamin D, parathyroid hormone, and mortality in black and white older adults: the health ABC study. J. Clin. Endocrinol. Metab. 2012;97(11):4156–65. DOI: 10.1210/jc.2012-1551
  • 16. Aydin, O., and Pehlivanli, F. Paratiroid Adenomunun Ameliyat Öncesi Tanısında Öngörücü Bir Biyobelirteç Olarak Trombosit/Lenfosit Oranı. Kırıkkale Üniversitesi Tıp Fakültesi Derg. 2019:73–79. DOI: 10.24938/kutfd.522955
  • 17. Li, W., Liu, Q., and Tang, Y. Platelet to lymphocyte ratio in the prediction of adverse outcomes after acute coronary syndrome: a meta-analysis. Sci. Rep. 2017;7(1):40426. DOI: 10.1038/srep40426
  • 18. Lippi, G., Targher, G., Montagnana, M., Salvagno, G.L., Zoppini, G., and Guidi, G.C. Relation between red blood cell distribution width and inflammatory biomarkers in a large cohort of unselected outpatients. Arch. Pathol. Lab. Med. 2009;133(4):628–32. DOI: 10.1043/1543-2165-133.4.628
  • 19. Christensen, M.H.E., Dankel, S.N., Nordbø, Y., Varhaug, J.E., Almås, B., Lien, E.A et al. Primary hyperparathyroidism influences the expression of inflammatory and metabolic genes in adipose tissue. PloS One 2011;6(6):e20481. PMID: 21698093
  • 20. Wu, C.-C., Chang, J.-H., Chen, C.-C., Su, S.-B., Yang, L.-K., Ma, W.-Y et al. Calcitriol treatment attenuates inflammation and oxidative stress in hemodialysis patients with secondary hyperparathyroidism. Tohoku J. Exp. Med. 2011;223(3):153–9. PMID: 21350317
  • 21. Zeren, S., Yaylak, F., Ozbay, I., and Bayhan, Z. Relationship Between the Neutrophil to Lymphocyte Ratio and Parathyroid Adenoma Size in Patients With Primary Hyperparathyroidism. Int. Surg. 100, 2015;100(7-8):1185–9. DOI: 10.9738/INTSURG-D-15-00044.1
  • 22. Ahbap, E., Sakaci, T., Kara, E., Sahutoglu, T., Koc, Y., Basturk, T et al. Neutrophil-to-lymphocyte ratio and platelet-tolymphocyte ratio in evaluation of inflammation in end-stage renal disease. Clin. Nephrol.2016; 85(4):199–208. DOI: 10.5414/CN108584
  • 23. Zhang, Q., Cao, X., Zhou, J., Ding, R., Huang, J., Cai, G et al. Red cell distribution width reflects the early stage residual renal function in peritoneal dialysis patients. Saudi J. Kidney Dis. Transplant. Off. Publ. Saudi Cent. Organ Transplant. Saudi Arab. 2018;29(5):1082–91. DOI: 10.4103/1319-2442.243950
  • 24. Perlstein, T.S., Weuve, J., Pfeffer, M.A., and Beckman, J.A. Red Blood Cell Distribution Width and Mortality Risk in a Community-Based Prospective Cohort. Arch. Intern. Med. 2009;169(6):588. DOI: 10.1001/archinternmed.2009.55
  • 25. Ayça, B., Akin, F., Çelik, Ö., Yüksel, Y., Öztürk, D., Tekiner, F et al. Platelet to lymphocyte ratio as a prognostic marker in primary percutaneous coronary intervention. Platelets 2015;26(7):638–44. DOI: 10.3109/09537104.2014.968117
There are 25 citations in total.

Details

Primary Language English
Subjects ​Internal Diseases
Journal Section Research Article
Authors

Selvihan Beysel 0000-0001-6963-1503

Mustafa Çalışkan 0000-0003-0342-571X

Muhammed Kızılgül 0000-0002-8468-9196

Murat Çilekar This is me 0000-0001-9175-6791

Mustafa Özbek This is me 0000-0003-1125-3823

Erman Çakal This is me 0000-0003-4455-7276

Publication Date October 26, 2019
Submission Date May 21, 2019
Acceptance Date August 3, 2019
Published in Issue Year 2019

Cite

Vancouver Beysel S, Çalışkan M, Kızılgül M, Çilekar M, Özbek M, Çakal E. Association between inflammatory markers and primary hyperparathyroidism. Acta Med. Alanya. 2019;3(3):241-7.

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