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Association between inflammatory markers and primary hyperparathyroidism

Year 2019, Volume: 3 Issue: 3, 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, Volume: 3 Issue: 3, 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 Volume: 3 Issue: 3

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.

9705

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