Skip to main content
Top
Published in: World Journal of Surgery 7/2007

01-07-2007

Serum Levels of Uric Acid and Diabetes Mellitus Influence Survival after Surgery for Primary Hyperparathyroidism: A Prospective Cohort Study

Authors: Anders Bergenfelz, Anna Bladström, Mark Their, Erik Nordenström, Stig Valdemarsson, Johan Westerdahl

Published in: World Journal of Surgery | Issue 7/2007

Login to get access

Abstract

Background

Primary hyperparathyroidism (pHPT) is associated with an increased mortality attributable to cardiovascular disease (CVD), suggested to be alleviated by surgery. The exact mechanism of the beneficial influence of parathyroidectomy on survival is unknown. Furthermore, studies suggest that there is no increased mortality compared to the mortality rate in the general population during recent years. This study therefore investigated relative survival (RS), as well overall mortality associated with the clinical and biochemical variables in patients undergoing operation for sporadic pHPT. Furthermore, the influence of surgery on biochemical variables associated with pHPT was analyzed.

Methods

A group of 323 patients with sporadic pHPT operated between September 1989 and July 2003 were followed from surgery over a 10-year period. The median and mean follow-up time was 69 and 70 months, respectively (range: 1–120 months). Relative survival (RS) was calculated, and the impact of clinical and biochemical variables on overall death were evaluated.

Results

Postoperatively, serum levels of triglycerides and uric acid decreased. Glucose levels and glomerular filtration rate remained unchanged. A decreased RS was evident during the latter part of the 10 year follow-up period. In the multivariate Cox-analysis, diabetes mellitus (hazard ratio [HR] = 2.8, 95%; confidence interval [CI] 1.2–6.7), and the combination of an increased level of serum uric acid and cardiovascular disease (CVD) (HR = 8.6, 95%; CI 1.5–49.7) was associated with a higher mortality. The increased risk of death was evident for patients with persistently increased levels of uric acid postoperatively (HR = 4.8, 95%; CI = 1.4–16.01)

Conclusions

Patients undergoing operation for pHPT had a decreased RS during a 10-year follow-up compared to the general population. This decrease in RS is associated with diabetes mellitus and increased levels of uric acid pre-and postoperatively.
Literature
1.
go back to reference Nilsson IL, Yin L, Lundgren E, et al. (2002) Clinical presentation of primary hyperparathyroidism in Europe—nationwide cohort analysis on mortality from nonmalignant causes. J Bone Miner Res 17 Suppl 2:N68–74 Nilsson IL, Yin L, Lundgren E, et al. (2002) Clinical presentation of primary hyperparathyroidism in Europe—nationwide cohort analysis on mortality from nonmalignant causes. J Bone Miner Res 17 Suppl 2:N68–74
2.
go back to reference Nilsson IL, Wadsten C, Brandt L, et al. (2004) Mortality in sporadic primary hyperparathyroidism: nationwide cohort study of multiple parathyroid gland disease. Surgery 136:981–987PubMedCrossRef Nilsson IL, Wadsten C, Brandt L, et al. (2004) Mortality in sporadic primary hyperparathyroidism: nationwide cohort study of multiple parathyroid gland disease. Surgery 136:981–987PubMedCrossRef
3.
go back to reference Ogard CG, Engholm G, Almdal TP, et al. (2004) Increased mortality in patients hospitalized with primary hyperparathyroidism during the period 1977–1993 in Denmark. World J Surg 28:108–111PubMedCrossRef Ogard CG, Engholm G, Almdal TP, et al. (2004) Increased mortality in patients hospitalized with primary hyperparathyroidism during the period 1977–1993 in Denmark. World J Surg 28:108–111PubMedCrossRef
4.
go back to reference Palmer M, Adami HO, Bergstrom R, et al. (1987) Mortality after surgery for primary hyperparathyroidism: a follow-up of 441 patients operated on from 1956 to 1979. Surgery 102:1–7PubMed Palmer M, Adami HO, Bergstrom R, et al. (1987) Mortality after surgery for primary hyperparathyroidism: a follow-up of 441 patients operated on from 1956 to 1979. Surgery 102:1–7PubMed
5.
go back to reference Vestergaard P, Mosekilde L (2003) Cohort study on effects of parathyroid surgery on multiple outcomes in primary hyperparathyroidism. BMJ 327:530–534PubMedCrossRef Vestergaard P, Mosekilde L (2003) Cohort study on effects of parathyroid surgery on multiple outcomes in primary hyperparathyroidism. BMJ 327:530–534PubMedCrossRef
6.
go back to reference Vestergaard P, Mollerup CL, Frokjaer VG, et al. (2003) Cardiovascular events before and after surgery for primary hyperparathyroidism. World J Surg 27:216–222PubMedCrossRef Vestergaard P, Mollerup CL, Frokjaer VG, et al. (2003) Cardiovascular events before and after surgery for primary hyperparathyroidism. World J Surg 27:216–222PubMedCrossRef
7.
go back to reference Hedback G, Oden A (1998) Increased risk of death from primary hyperparathyroidism—an update. Eur J Clin Invest 28:271–276PubMedCrossRef Hedback G, Oden A (1998) Increased risk of death from primary hyperparathyroidism—an update. Eur J Clin Invest 28:271–276PubMedCrossRef
8.
go back to reference Leifsson BG, Ahren B (1996) Serum calcium and survival in a large health screening program. J Clin Endocrinol Metab 81:2149–2153PubMedCrossRef Leifsson BG, Ahren B (1996) Serum calcium and survival in a large health screening program. J Clin Endocrinol Metab 81:2149–2153PubMedCrossRef
9.
go back to reference Lundgren E, Lind L, Palmer M, et al. (2001) Increased cardiovascular mortality and normalized serum calcium in patients with mild hypercalcemia followed up for 25 years. Surgery 130:978–985PubMedCrossRef Lundgren E, Lind L, Palmer M, et al. (2001) Increased cardiovascular mortality and normalized serum calcium in patients with mild hypercalcemia followed up for 25 years. Surgery 130:978–985PubMedCrossRef
10.
go back to reference Hedback G, Oden A, Tisell LE (1991) The influence of surgery on the risk of death in patients with primary hyperparathyroidism. World J Surg 15:399–405; discussion 406–407PubMedCrossRef Hedback G, Oden A, Tisell LE (1991) The influence of surgery on the risk of death in patients with primary hyperparathyroidism. World J Surg 15:399–405; discussion 406–407PubMedCrossRef
11.
go back to reference Hedback G, Oden A (1998) Death risk factor analysis in primary hypeparathyroidism. Eur J Clin Invest 28:1011–1018PubMedCrossRef Hedback G, Oden A (1998) Death risk factor analysis in primary hypeparathyroidism. Eur J Clin Invest 28:1011–1018PubMedCrossRef
12.
go back to reference Bergenfelz A, Isaksson A, Ahren B (1994) Intraoperative monitoring of intact PTH during surgery for primary hyperparathyroidism. Langenbecks Arch Chir 379:50–53PubMed Bergenfelz A, Isaksson A, Ahren B (1994) Intraoperative monitoring of intact PTH during surgery for primary hyperparathyroidism. Langenbecks Arch Chir 379:50–53PubMed
13.
go back to reference World Health Organization-International Society of Hypertension Guidelines for the Management of Hypertension (1999) Guidelines Subcommittee. J Hypertens 17:151–183 World Health Organization-International Society of Hypertension Guidelines for the Management of Hypertension (1999) Guidelines Subcommittee. J Hypertens 17:151–183
14.
go back to reference Krutzen E, Back SE, Nilsson-Ehle I, et al. (1984) Plasma clearance of a new contrast agent, iohexol: a method for the assessment of glomerular filtration rate. J Lab Clin Med 104:955–961PubMed Krutzen E, Back SE, Nilsson-Ehle I, et al. (1984) Plasma clearance of a new contrast agent, iohexol: a method for the assessment of glomerular filtration rate. J Lab Clin Med 104:955–961PubMed
15.
go back to reference Hedback G, Oden A, Tisell LE (1995) Parathyroid adenoma weight and the risk of death after treatment for primary hyperparathyroidism. Surgery 117:134–139PubMedCrossRef Hedback G, Oden A, Tisell LE (1995) Parathyroid adenoma weight and the risk of death after treatment for primary hyperparathyroidism. Surgery 117:134–139PubMedCrossRef
16.
go back to reference Hedback G, Oden A (1995) Clinical evaluation of total serum calcium in primary hyperparathyroidism and the risk of death after surgery. Eur J Clin Invest 25:48– 52PubMed Hedback G, Oden A (1995) Clinical evaluation of total serum calcium in primary hyperparathyroidism and the risk of death after surgery. Eur J Clin Invest 25:48– 52PubMed
17.
go back to reference Ljunghall S, Palmer M, Akerstrom G, et al. (1983) Diabetes mellitus, glucose tolerance and insulin response to glucose in patients with primary hyperparathyroidism before and after parathyroidectomy. Eur J Clin Invest 13:373–377PubMedCrossRef Ljunghall S, Palmer M, Akerstrom G, et al. (1983) Diabetes mellitus, glucose tolerance and insulin response to glucose in patients with primary hyperparathyroidism before and after parathyroidectomy. Eur J Clin Invest 13:373–377PubMedCrossRef
18.
go back to reference Procopio M, Magro G, Cesario F, et al. (2002) The oral glucose tolerance test reveals a high frequency of both impaired glucose tolerance and undiagnosed type 2 diabetes mellitus in primary hyperparathyroidism. Diabet Med 19:958–961PubMedCrossRef Procopio M, Magro G, Cesario F, et al. (2002) The oral glucose tolerance test reveals a high frequency of both impaired glucose tolerance and undiagnosed type 2 diabetes mellitus in primary hyperparathyroidism. Diabet Med 19:958–961PubMedCrossRef
19.
go back to reference Valdermarsson S, Leckstrom A, Westermark P, et al. (1996) Increased plasma levels of islet amyloid polypeptide in patients with primary hyperparathyroidism. Eur J Endocrinol 134:320–325PubMed Valdermarsson S, Leckstrom A, Westermark P, et al. (1996) Increased plasma levels of islet amyloid polypeptide in patients with primary hyperparathyroidism. Eur J Endocrinol 134:320–325PubMed
20.
go back to reference Hagstrom E, Lundgren E, Lithell H, et al. (2002) Normalized dyslipidaemia after parathyroidectomy in mild primary hyperparathyroidism: population-based study over five years. Clin Endocrinol (Oxf) 56:253–260CrossRef Hagstrom E, Lundgren E, Lithell H, et al. (2002) Normalized dyslipidaemia after parathyroidectomy in mild primary hyperparathyroidism: population-based study over five years. Clin Endocrinol (Oxf) 56:253–260CrossRef
21.
go back to reference Lundgren E, Ljunghall S, Akerstrom G, et al. (1998) Case-control study on symptoms and signs of “asymptomatic” primary hyperparathyroidism. Surgery 124:980–985; discussion 985–986PubMed Lundgren E, Ljunghall S, Akerstrom G, et al. (1998) Case-control study on symptoms and signs of “asymptomatic” primary hyperparathyroidism. Surgery 124:980–985; discussion 985–986PubMed
22.
go back to reference Ljunghall S, Akerstrom G (1982) Urate metabolism in primary hyperparathyroidism. Urol Int 37:73–78PubMedCrossRef Ljunghall S, Akerstrom G (1982) Urate metabolism in primary hyperparathyroidism. Urol Int 37:73–78PubMedCrossRef
23.
go back to reference Pepersack T, Jabbour N, Fuss M, et al. (1989) Hyperuricemia and renal handling of urate in primary hyperparathyroidism. Nephron 53:349–352PubMedCrossRef Pepersack T, Jabbour N, Fuss M, et al. (1989) Hyperuricemia and renal handling of urate in primary hyperparathyroidism. Nephron 53:349–352PubMedCrossRef
24.
go back to reference Duh QY, Morris RC, Arnaud CD, et al. (1986) Decrease in serum uric acid level following parathyroidectomy in patients with primary hyperparathyroidism. World J Surg 10:729–736PubMedCrossRef Duh QY, Morris RC, Arnaud CD, et al. (1986) Decrease in serum uric acid level following parathyroidectomy in patients with primary hyperparathyroidism. World J Surg 10:729–736PubMedCrossRef
25.
go back to reference Broulik PD, Stepan JJ, Pacovsky V (1987) Primary hyperparathyroidism and hyperuricaemia are associated but not correlated with indicators of bone turnover. Clin Chim Acta 170:195–200PubMedCrossRef Broulik PD, Stepan JJ, Pacovsky V (1987) Primary hyperparathyroidism and hyperuricaemia are associated but not correlated with indicators of bone turnover. Clin Chim Acta 170:195–200PubMedCrossRef
26.
go back to reference Bolland MJ, Grey AB, Gamble GD, et al. (2005) Association between primary hyperparathyroidism and increased body weight: a meta-analysis. J Clin Endocrinol Metab 90:1525–1530PubMedCrossRef Bolland MJ, Grey AB, Gamble GD, et al. (2005) Association between primary hyperparathyroidism and increased body weight: a meta-analysis. J Clin Endocrinol Metab 90:1525–1530PubMedCrossRef
27.
go back to reference Prager R, Schernthaner G, Niederle B, et al. (1990) Evaluation of glucose tolerance, insulin secretion, and insulin action in patients with primary hyperparathyroidism before and after surgery. Calcif Tissue Int 46:1–4PubMedCrossRef Prager R, Schernthaner G, Niederle B, et al. (1990) Evaluation of glucose tolerance, insulin secretion, and insulin action in patients with primary hyperparathyroidism before and after surgery. Calcif Tissue Int 46:1–4PubMedCrossRef
28.
go back to reference Bannon MP, van Heerden JA, Palumbo PJ, et al. (1988) The relationship between primary hyperparathyroidism and diabetes mellitus. Ann Surg 207:430–433PubMedCrossRef Bannon MP, van Heerden JA, Palumbo PJ, et al. (1988) The relationship between primary hyperparathyroidism and diabetes mellitus. Ann Surg 207:430–433PubMedCrossRef
29.
go back to reference Bickel C, Rupprecht HJ, Blankenberg S et al. (2002) Serum uric acid as an independent predictor of mortality in patients with angiographically proven coronary artery disease. Am J Cardiol 89:12–17PubMedCrossRef Bickel C, Rupprecht HJ, Blankenberg S et al. (2002) Serum uric acid as an independent predictor of mortality in patients with angiographically proven coronary artery disease. Am J Cardiol 89:12–17PubMedCrossRef
30.
go back to reference Fang J, Alderman MH (2000) Serum uric acid and cardiovascular mortality the NHANES I epidemiologic follow-up study, 1971–1992. National Health and Nutrition Examination Survey. JAMA 283:2404–2410PubMedCrossRef Fang J, Alderman MH (2000) Serum uric acid and cardiovascular mortality the NHANES I epidemiologic follow-up study, 1971–1992. National Health and Nutrition Examination Survey. JAMA 283:2404–2410PubMedCrossRef
31.
go back to reference Franse LV, Pahor M, Di Bari M, et al. (2000) Serum uric acid, diuretic treatment and risk of cardiovascular events in the Systolic Hypertension in the Elderly Program (SHEP). J Hypertens 18:1149–1154PubMedCrossRef Franse LV, Pahor M, Di Bari M, et al. (2000) Serum uric acid, diuretic treatment and risk of cardiovascular events in the Systolic Hypertension in the Elderly Program (SHEP). J Hypertens 18:1149–1154PubMedCrossRef
32.
go back to reference Hoieggen A, Alderman MH, Kjeldsen SE, et al. (2004) The impact of serum uric acid on cardiovascular outcomes in the LIFE study. Kidney Int 65:1041–1049PubMedCrossRef Hoieggen A, Alderman MH, Kjeldsen SE, et al. (2004) The impact of serum uric acid on cardiovascular outcomes in the LIFE study. Kidney Int 65:1041–1049PubMedCrossRef
33.
go back to reference Liese AD, Hense HW, Lowel H, et al. (1999) Association of serum uric acid with all-cause and cardiovascular disease mortality and incident myocardial infarction in the MONICA Augsburg cohort. World Health Organization Monitoring Trends and Determinants in Cardiovascular Diseases. Epidemiology 10:391–397PubMedCrossRef Liese AD, Hense HW, Lowel H, et al. (1999) Association of serum uric acid with all-cause and cardiovascular disease mortality and incident myocardial infarction in the MONICA Augsburg cohort. World Health Organization Monitoring Trends and Determinants in Cardiovascular Diseases. Epidemiology 10:391–397PubMedCrossRef
34.
go back to reference Verdecchia P, Schillaci G, Reboldi G, et al. (2000) Relation between serum uric acid and risk of cardiovascular disease in essential hypertension. The PIUMA study. Hypertension 36:1072–1078 Verdecchia P, Schillaci G, Reboldi G, et al. (2000) Relation between serum uric acid and risk of cardiovascular disease in essential hypertension. The PIUMA study. Hypertension 36:1072–1078
35.
go back to reference Weir CJ, Muir SW, Walters MR, et al. (2003) Serum urate as an independent predictor of poor outcome and future vascular events after acute stroke. Stroke 34:1951–1956PubMedCrossRef Weir CJ, Muir SW, Walters MR, et al. (2003) Serum urate as an independent predictor of poor outcome and future vascular events after acute stroke. Stroke 34:1951–1956PubMedCrossRef
36.
go back to reference Wong KY, MacWalter RS, Fraser HW, et al. (2002) Urate predicts subsequent cardiac death in stroke survivors. Eur Heart J 23:788–793PubMedCrossRef Wong KY, MacWalter RS, Fraser HW, et al. (2002) Urate predicts subsequent cardiac death in stroke survivors. Eur Heart J 23:788–793PubMedCrossRef
37.
go back to reference Baker JF, Krishnan E, Chen L, et al. (2005) Serum uric acid and cardiovascular disease: recent developments, and where do they leave us? Am J Med 118:816–826PubMedCrossRef Baker JF, Krishnan E, Chen L, et al. (2005) Serum uric acid and cardiovascular disease: recent developments, and where do they leave us? Am J Med 118:816–826PubMedCrossRef
38.
go back to reference Madsen TE, Muhlestein JB, Carlquist JF, et al. (2005) Serum uric acid independently predicts mortality in patients with significant, angiographically defined coronary disease. Am J Nephrol 25:45–49PubMedCrossRef Madsen TE, Muhlestein JB, Carlquist JF, et al. (2005) Serum uric acid independently predicts mortality in patients with significant, angiographically defined coronary disease. Am J Nephrol 25:45–49PubMedCrossRef
39.
go back to reference Short RA, Johnson RJ, Tuttle KR (2005) Uric acid, microalbuminuria and cardiovascular events in high-risk patients. Am J Nephrol 25:36–44PubMedCrossRef Short RA, Johnson RJ, Tuttle KR (2005) Uric acid, microalbuminuria and cardiovascular events in high-risk patients. Am J Nephrol 25:36–44PubMedCrossRef
40.
go back to reference Alderman M, Aiyer KJ (2004) Uric acid: role in cardiovascular disease and effects of losartan. Curr Med Res Opin 20:369–379PubMedCrossRef Alderman M, Aiyer KJ (2004) Uric acid: role in cardiovascular disease and effects of losartan. Curr Med Res Opin 20:369–379PubMedCrossRef
Metadata
Title
Serum Levels of Uric Acid and Diabetes Mellitus Influence Survival after Surgery for Primary Hyperparathyroidism: A Prospective Cohort Study
Authors
Anders Bergenfelz
Anna Bladström
Mark Their
Erik Nordenström
Stig Valdemarsson
Johan Westerdahl
Publication date
01-07-2007
Publisher
Springer-Verlag
Published in
World Journal of Surgery / Issue 7/2007
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-007-9091-6

Other articles of this Issue 7/2007

World Journal of Surgery 7/2007 Go to the issue