- Email: [email protected]
Prevalence of Zinc Deficiency in Cardiac Surgery Patients
HLC 2460 No. of Pages 3
BRIEF COMMUNICATION
Heart, Lung and Circulation (2017) xx, 1–3 1443-9506/04/$36.00 http://dx.doi.org/10.1016/j.hlc.2017.07.009
Prevalence of Zinc Deficiency in Cardiac Surgery Patients Lesley A. Braun, PhD a[3_TD$IF],b, Ruchong Ou, MBBS, MD c, Christina Kure, PhD d[32_TD$IF], Adriana Trang, MBBS, B Pharm c, Franklin Rosenfeldt, MD, FRACS e,f* a
Monash/Alfred Psychiatry Research Centre, Alfred Hospital, Melbourne, Vic, Australia The National Institute of Complementary Medicine, University of Western Sydney, Sydney, NSW, Australia Department of Surgery, Monash University, Melbourne, Vic, Australia d Department of Cardiothoracic Surgery, Alfred Hospital, Melbourne, Vic, Australia e Baker Heart and Diabetes Institute, Melbourne, Vic, Australia f Faculty of Health, Arts and Design, Swinburne University [34_TD$IF]of Technology, Melbourne, Vic, Australia b c
Received 3 May 2017; received in revised form 22 June 2017; accepted 26 July 2017; online published-ahead-of-print xxx
Background
The aim of this study was to define the status of preoperative zinc levels in patients with heart disease presenting for cardiac surgery and to identify any predictors for and any clinical consequences of low zinc levels.
Methods
Adult patients presenting for elective surgery, either coronary artery bypass graft surgery and/or valve replacement, provided a fasting blood sample on the day of admission for surgery. Plasma and erythrocyte zinc levels were analysed and the levels correlated with the patient’s characteristics and clinical outcomes.
Results
Of 56 patients 53% (n = 30) had abnormally low plasma zinc levels (<12 m [37_TD$IF] mol/L) and 5.5% (n = 3) had abnormally low erythrocyte zinc levels (<160 [37_TD$IF]mmol/L), indicative of deficiency. There were significant associations between lower plasma zinc levels and the presence of hypertension (p = 0.02), hypercholesteraemia (p = 0.02) and higher body mass index (BMI) (p = 0.034) but no effect on major postoperative clinical outcomes.
Conclusions
This small study shows that zinc deficiency is common in cardiac surgery patients, especially in the presence of hypertension, hypercholesterolaemia or obesity. The effects of zinc deficiency in cardiac surgery need to be further investigated.
Keywords
Zinc deficiency Cardiovascular disease Cardiac surgery Complementary medicine
Introduction
Methods
Zinc deficiency can adversely affect critically ill patients [1]. There is a paucity of information about the prevalence of zinc levels in cardiac surgery patients. The aim of this study was to define the status of preoperative zinc levels in patients presenting for cardiac surgery and to identify preoperative predictors, or major postoperative clinical consequences, of low zinc levels.
A prospective study was conducted at The Alfred Hospital, Melbourne, Australia. Ethical approval was received from the Alfred Hospital Human Research Ethics Committee and the study was conducted according the Declaration of Helsinki. Fifty-six elective cardiac surgery patients aged 18 years and above, attending the pre-admission clinic were
*Corresponding author at: Baker Heart and Diabetes Institute, 75 Commercial Road, Melbourne 3004, Australia. Tel.: 03 9857 6036, Mobile: 61 408 150 521., Email: [email protected] © 2017 Australian and New Zealand Society of Cardiac and Thoracic Surgeons (ANZSCTS) and the Cardiac Society of Australia and New Zealand (CSANZ). Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Braun LA, et al. Prevalence of Zinc Deficiency in Cardiac Surgery Patients. Heart, Lung and Circulation (2017), http://dx.doi.org/10.1016/j.hlc.2017.07.009
HLC 2460 No. of Pages 3
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L.A. Braun et al.
prospectively enrolled in the study. A fasting venous blood sample was collected prior to surgery. Plasma zinc was assayed using the Flame Atomic Absorption Spectrophotometry method and erythrocyte zinc was analysed using GBC Atomic Absorption Spectroscopy [2]. Plasma zinc deficiency was defined as plasma zinc below 12 mmol/L and erythrocyte zinc deficiency levels below 160 mmol/L [3,4]. The condition of the patients on admission to the ICU after surgery was measured and scored by ICU staff using the standard Acute Physiology and Chronic Health Evaluation III (APACHE III) method [5]. Data was initially assessed for normality with normally distributed variables presented as mean (standard deviation) and non-normally distributed variables presented as median (interquartile range). The student’s t test was used for parametric and the Mann Whitney u-test for non-parametric variables. Univariate relationships between zinc levels and independent variables were determined using linear regression with results reported as parameter estimates (standard error) and R-square. A p-value of [38_TD$IF]<0.05 was considered to be statistically significant.
Results Fifty-six patients were enrolled (Table 1) Of the total cohort, 53% (n = 30) had abnormally low plasma zinc levels (<12 mmol/L) and 5.5% (n = 3) were had abnormally low erythrocyte zinc levels (<160 mmol/L). There were significant univariate associations between lower plasma zinc levels and higher BMI ( 0.06 (0.03) R2[3_TD$IF] = 8 [39_TD$IF]p = 0.03), hypertension and hypercholesterolaemia (1.68 (0.71) R2 = 9.4 [40_TD$IF]p = 0.02). No significant associations were observed between plasma zinc and age or diabetes. When the patients with zinc deficiency (plasma levels below 12 mmol/L) were compared to those with adequate zinc status, no significant differences were found in mortality, APACHE III scores, or length of stay in ICU or hospital (Table 2).
Discussion In this prospective observational study of elective cardiac surgery patients, we found a high prevalence of zinc
Table 1 Patient characteristics and medications (n = 56). n (%) Clinical characteristics and medications Obesity: BMI > 30 kg/m2
32 (57%)
Diabetes
15 (27%)
Coronary artery disease (age 63.5 2.1)
23 (41%)
Valvular heart disease (age 69.4 2.2) Coronary artery disease + valvular
20 (36%) 13 (23%)
disease (age 71.5 2.8) Medications: Anti-hypertensives
47 (84%)
Angiotensin II receptor blockers
13 (23%)
Angiotensin converting enzyme inhibitors
24 (43%)
deficiency in plasma and, to a lesser extent, in red blood cells. More than half of the patients had plasma zinc levels below 12 mmol/L. We also found lower plasma zinc levels were associated with obesity, with hypertension and hypercholesterolaemia. There were no associations between low zinc levels and major adverse postoperative outcomes. The postoperative outcomes we recorded were unaffected by zinc status but these are known to be strongly impacted upon by a multitude of non-nutritional factors. Zinc is an essential trace element known for its role in immune system [6] and in many metabolic processes including reduction of oxidative stress. Although zinc does not have direct antioxidant activity, it contributes to the free radical defence mechanisms of the body by binding to thiol groups in proteins making them less susceptible to oxidation [7]. This has particular relevance for cardiac surgery patients who experience ischaemia-reperfusion injury and oxidative stress during and after surgery and where zinc-dependent antioxidants are required [8]. The zinc pool in plasma is relatively small, representing only about 0.1% of total body zinc [9]. Five-fold greater amounts of zinc are found in whole blood than in plasma [10]. Zinc deficiency can adversely affect critically ill patients [1]. A previous study found that a low serum zinc level in
Table 2 Postoperative results and plasma zinc. Variable
Plasma zinc levels All patients (n = 56)
p-Value Normal: 12 mmol/L (n = 26)
Low: <12 mmol/L (n = 30)
Mortality (30 day)
0
0
0
–
APACHE III
45 [36–51]
48 [38–54]
44 [35–49]
0.10
Intensive care unit stay (hours)
42 [28–70]
42 [25–73]
42 [29–65]
0.65
Hospital stay (days)
7 [6–10.5]
7.5 [6–11]
7 [31_TD$IF][6–10]
0.37
Data expressed as median [interquartile range]. Abbreviation: APACHE III = Acute Physiology and Chronic Health Evaluation III.
Please cite this article in press as: Braun LA, et al. Prevalence of Zinc Deficiency in Cardiac Surgery Patients. Heart, Lung and Circulation (2017), http://dx.doi.org/10.1016/j.hlc.2017.07.009
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Prevalence of Zinc Deficiency
patients on presentation to the intensive care unit was associated with multi-organ failure [11]. Critical illness itself can lead to a decline in serum zinc concentrations [1]. Cardiac surgery patients may be at particular risk of zinc deficiency as they tend to be older, with concomitant obesity, hypertension, hyperlipidaemia, diabetes mellitus, and heart failure. The high prevalence of zinc deficiency which we have observed may be related to the study population of cardiac surgery patients many of whom were taking antihypertensive medications such as angiotensin converting enzyme inhibitors or angiotensin receptor blockers both of which we [12] and others [13] have shown to reduce zinc levels via increased urinary losses. The present study has noted that high BMI may also be a predictor of zinc deficiency. This may relate to possible relationship of the serum zinc levels with the anabolic and catabolic mechanisms in obesity. It has been reported in human trials that zinc concentrations were negatively associated with BMI indicating that zinc may be playing a role in fat deposition of obesity [14].
Conclusions This study shows that zinc deficiency is common in cardiac surgery patients, especially in the presence of hypertension, hypercholesterolaemia or obesity. Although an association between zinc deficiency and postoperative outcomes was not established, the adverse effect of lower zinc on cardiac surgical patients deserves further investigation.
Disclosures LB and FR have received research funding from [41_TD$IF]Blackmores.
References [1] Cander B, Dundar ZD, Gul M, Girisgin S. Prognostic value of serum zinc levels in critically ill patients. J Crit Care 2011;26(Feb (1)):42–6. [2] Dutra RL, Cantos GA, Carasek E. Analysis of zinc in biological samples by flame atomic absorption spectrometry: use of addition calibration technique. Biol Trace Elem Res 2006;111(1–3):265–79. [3] Hotz C, Peerson JM, Brown KH. Suggested lower cutoffs of serum zinc concentrations for assessing zinc status: reanalysis of the second National Health and Nutrition Examination Survey data. Am J Clin Nutr 2003;78:756–64. [4] Tiran B, Lorenz O, Tiran A, Buchinger W, Eber O. Comparison of direct versus indirect determination of zinc concentration in erythrocytes in euthyroid and hyperthyroid subjects. Eur J Clin Chem Clin Biochem 1993;31:239–44. [5] Knaus WA, Wagner DP, Draper EA, Zimmerman JE, Bergner M, Bastos PG, et al. The APACHE III prognostic system. Risk prediction of hospital mortality for critically ill hospitalized adults. Chest 1991;100(6):1619–36. [6] Prasad AS. Zinc in Human Health: Effect of Zinc on Immune Cells. Mol Med 2008;14(May–Jun (5–6)):353–7. [7] Prasad AS, Beck FWJ, Bao B, Snell DC, Steinberg JD, Cardozo LJ. Zinc supplementation decreases incidence of infections in the elderly: Effect of zinc on generation of cytokines and oxidative stress. Am J Clin Nutr 2007;85:837–44. [8] Clermont G, Vergely C, Jazayeri S, Lahet JJ, Goudeau JJ, Lecour S. Systemic Free Radical Activation Is a Major Event Involved In Myocardial Oxidative Stress Related to Cardiopulmonary Bypass. Anesthesiology 2002;96:80–7. [9] Roohani N, Hurrell R, Kelishadi R, Schulin R. Zinc and its importance for human health: An integrative review. J Res Med Sci 2013;18(Feb (2)):144–57. [10] Buxaderas SC, Farre´-Rovira R. Whole blood and serum zinc levels in relation to sex and age. Rev Esp Fisiol 1985;41(Dec (4)):463–70. [11] Linko R, Karlsson S, Pettila¨ V, Varpula T, Okkonen M, et al. Serum zinc in critically ill adult patients with acute respiratory failure. Acta Anaesthesiol Scand 2011;55(May (5)):615–21. [12] Braun LA, Rosenfeldt F. Pharmaco-nutrient interactions: – a systematic review of zinc and antihypertensive therapy. Int J Clin Pract 2013;67 (August (8)):717–25. [13] Koren-Michowitz M, Dishy V, Zaidenstein R, Yona O, Berman S, Weissgarten J, et al. The effect of losartan and losartan/hydrochlorothiazide fixed-combination on magnesium, zinc, and nitric oxide metabolism in hypertensive patients: a prospective open-label study. Am J Hypertens 2005;18(3):358–63. [14] Garcı´a OP, Ronquillo D, Caaman˜o M, Camacho M, Long KZ, Rosado JL. Zinc, vitamin A, and vitamin C status are associated with leptin concentrations and obesity in Mexican women: results from a cross-sectional study. Nutr Metab 2012;9:59.
Please cite this article in press as: Braun LA, et al. Prevalence of Zinc Deficiency in Cardiac Surgery Patients. Heart, Lung and Circulation (2017), http://dx.doi.org/10.1016/j.hlc.2017.07.009
BRIEF COMMUNICATION
Heart, Lung and Circulation (2017) xx, 1–3 1443-9506/04/$36.00 http://dx.doi.org/10.1016/j.hlc.2017.07.009
Prevalence of Zinc Deficiency in Cardiac Surgery Patients Lesley A. Braun, PhD a[3_TD$IF],b, Ruchong Ou, MBBS, MD c, Christina Kure, PhD d[32_TD$IF], Adriana Trang, MBBS, B Pharm c, Franklin Rosenfeldt, MD, FRACS e,f* a
Monash/Alfred Psychiatry Research Centre, Alfred Hospital, Melbourne, Vic, Australia The National Institute of Complementary Medicine, University of Western Sydney, Sydney, NSW, Australia Department of Surgery, Monash University, Melbourne, Vic, Australia d Department of Cardiothoracic Surgery, Alfred Hospital, Melbourne, Vic, Australia e Baker Heart and Diabetes Institute, Melbourne, Vic, Australia f Faculty of Health, Arts and Design, Swinburne University [34_TD$IF]of Technology, Melbourne, Vic, Australia b c
Received 3 May 2017; received in revised form 22 June 2017; accepted 26 July 2017; online published-ahead-of-print xxx
Background
The aim of this study was to define the status of preoperative zinc levels in patients with heart disease presenting for cardiac surgery and to identify any predictors for and any clinical consequences of low zinc levels.
Methods
Adult patients presenting for elective surgery, either coronary artery bypass graft surgery and/or valve replacement, provided a fasting blood sample on the day of admission for surgery. Plasma and erythrocyte zinc levels were analysed and the levels correlated with the patient’s characteristics and clinical outcomes.
Results
Of 56 patients 53% (n = 30) had abnormally low plasma zinc levels (<12 m [37_TD$IF] mol/L) and 5.5% (n = 3) had abnormally low erythrocyte zinc levels (<160 [37_TD$IF]mmol/L), indicative of deficiency. There were significant associations between lower plasma zinc levels and the presence of hypertension (p = 0.02), hypercholesteraemia (p = 0.02) and higher body mass index (BMI) (p = 0.034) but no effect on major postoperative clinical outcomes.
Conclusions
This small study shows that zinc deficiency is common in cardiac surgery patients, especially in the presence of hypertension, hypercholesterolaemia or obesity. The effects of zinc deficiency in cardiac surgery need to be further investigated.
Keywords
Zinc deficiency Cardiovascular disease Cardiac surgery Complementary medicine
Introduction
Methods
Zinc deficiency can adversely affect critically ill patients [1]. There is a paucity of information about the prevalence of zinc levels in cardiac surgery patients. The aim of this study was to define the status of preoperative zinc levels in patients presenting for cardiac surgery and to identify preoperative predictors, or major postoperative clinical consequences, of low zinc levels.
A prospective study was conducted at The Alfred Hospital, Melbourne, Australia. Ethical approval was received from the Alfred Hospital Human Research Ethics Committee and the study was conducted according the Declaration of Helsinki. Fifty-six elective cardiac surgery patients aged 18 years and above, attending the pre-admission clinic were
*Corresponding author at: Baker Heart and Diabetes Institute, 75 Commercial Road, Melbourne 3004, Australia. Tel.: 03 9857 6036, Mobile: 61 408 150 521., Email: [email protected] © 2017 Australian and New Zealand Society of Cardiac and Thoracic Surgeons (ANZSCTS) and the Cardiac Society of Australia and New Zealand (CSANZ). Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Braun LA, et al. Prevalence of Zinc Deficiency in Cardiac Surgery Patients. Heart, Lung and Circulation (2017), http://dx.doi.org/10.1016/j.hlc.2017.07.009
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L.A. Braun et al.
prospectively enrolled in the study. A fasting venous blood sample was collected prior to surgery. Plasma zinc was assayed using the Flame Atomic Absorption Spectrophotometry method and erythrocyte zinc was analysed using GBC Atomic Absorption Spectroscopy [2]. Plasma zinc deficiency was defined as plasma zinc below 12 mmol/L and erythrocyte zinc deficiency levels below 160 mmol/L [3,4]. The condition of the patients on admission to the ICU after surgery was measured and scored by ICU staff using the standard Acute Physiology and Chronic Health Evaluation III (APACHE III) method [5]. Data was initially assessed for normality with normally distributed variables presented as mean (standard deviation) and non-normally distributed variables presented as median (interquartile range). The student’s t test was used for parametric and the Mann Whitney u-test for non-parametric variables. Univariate relationships between zinc levels and independent variables were determined using linear regression with results reported as parameter estimates (standard error) and R-square. A p-value of [38_TD$IF]<0.05 was considered to be statistically significant.
Results Fifty-six patients were enrolled (Table 1) Of the total cohort, 53% (n = 30) had abnormally low plasma zinc levels (<12 mmol/L) and 5.5% (n = 3) were had abnormally low erythrocyte zinc levels (<160 mmol/L). There were significant univariate associations between lower plasma zinc levels and higher BMI ( 0.06 (0.03) R2[3_TD$IF] = 8 [39_TD$IF]p = 0.03), hypertension and hypercholesterolaemia (1.68 (0.71) R2 = 9.4 [40_TD$IF]p = 0.02). No significant associations were observed between plasma zinc and age or diabetes. When the patients with zinc deficiency (plasma levels below 12 mmol/L) were compared to those with adequate zinc status, no significant differences were found in mortality, APACHE III scores, or length of stay in ICU or hospital (Table 2).
Discussion In this prospective observational study of elective cardiac surgery patients, we found a high prevalence of zinc
Table 1 Patient characteristics and medications (n = 56). n (%) Clinical characteristics and medications Obesity: BMI > 30 kg/m2
32 (57%)
Diabetes
15 (27%)
Coronary artery disease (age 63.5 2.1)
23 (41%)
Valvular heart disease (age 69.4 2.2) Coronary artery disease + valvular
20 (36%) 13 (23%)
disease (age 71.5 2.8) Medications: Anti-hypertensives
47 (84%)
Angiotensin II receptor blockers
13 (23%)
Angiotensin converting enzyme inhibitors
24 (43%)
deficiency in plasma and, to a lesser extent, in red blood cells. More than half of the patients had plasma zinc levels below 12 mmol/L. We also found lower plasma zinc levels were associated with obesity, with hypertension and hypercholesterolaemia. There were no associations between low zinc levels and major adverse postoperative outcomes. The postoperative outcomes we recorded were unaffected by zinc status but these are known to be strongly impacted upon by a multitude of non-nutritional factors. Zinc is an essential trace element known for its role in immune system [6] and in many metabolic processes including reduction of oxidative stress. Although zinc does not have direct antioxidant activity, it contributes to the free radical defence mechanisms of the body by binding to thiol groups in proteins making them less susceptible to oxidation [7]. This has particular relevance for cardiac surgery patients who experience ischaemia-reperfusion injury and oxidative stress during and after surgery and where zinc-dependent antioxidants are required [8]. The zinc pool in plasma is relatively small, representing only about 0.1% of total body zinc [9]. Five-fold greater amounts of zinc are found in whole blood than in plasma [10]. Zinc deficiency can adversely affect critically ill patients [1]. A previous study found that a low serum zinc level in
Table 2 Postoperative results and plasma zinc. Variable
Plasma zinc levels All patients (n = 56)
p-Value Normal: 12 mmol/L (n = 26)
Low: <12 mmol/L (n = 30)
Mortality (30 day)
0
0
0
–
APACHE III
45 [36–51]
48 [38–54]
44 [35–49]
0.10
Intensive care unit stay (hours)
42 [28–70]
42 [25–73]
42 [29–65]
0.65
Hospital stay (days)
7 [6–10.5]
7.5 [6–11]
7 [31_TD$IF][6–10]
0.37
Data expressed as median [interquartile range]. Abbreviation: APACHE III = Acute Physiology and Chronic Health Evaluation III.
Please cite this article in press as: Braun LA, et al. Prevalence of Zinc Deficiency in Cardiac Surgery Patients. Heart, Lung and Circulation (2017), http://dx.doi.org/10.1016/j.hlc.2017.07.009
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Prevalence of Zinc Deficiency
patients on presentation to the intensive care unit was associated with multi-organ failure [11]. Critical illness itself can lead to a decline in serum zinc concentrations [1]. Cardiac surgery patients may be at particular risk of zinc deficiency as they tend to be older, with concomitant obesity, hypertension, hyperlipidaemia, diabetes mellitus, and heart failure. The high prevalence of zinc deficiency which we have observed may be related to the study population of cardiac surgery patients many of whom were taking antihypertensive medications such as angiotensin converting enzyme inhibitors or angiotensin receptor blockers both of which we [12] and others [13] have shown to reduce zinc levels via increased urinary losses. The present study has noted that high BMI may also be a predictor of zinc deficiency. This may relate to possible relationship of the serum zinc levels with the anabolic and catabolic mechanisms in obesity. It has been reported in human trials that zinc concentrations were negatively associated with BMI indicating that zinc may be playing a role in fat deposition of obesity [14].
Conclusions This study shows that zinc deficiency is common in cardiac surgery patients, especially in the presence of hypertension, hypercholesterolaemia or obesity. Although an association between zinc deficiency and postoperative outcomes was not established, the adverse effect of lower zinc on cardiac surgical patients deserves further investigation.
Disclosures LB and FR have received research funding from [41_TD$IF]Blackmores.
References [1] Cander B, Dundar ZD, Gul M, Girisgin S. Prognostic value of serum zinc levels in critically ill patients. J Crit Care 2011;26(Feb (1)):42–6. [2] Dutra RL, Cantos GA, Carasek E. Analysis of zinc in biological samples by flame atomic absorption spectrometry: use of addition calibration technique. Biol Trace Elem Res 2006;111(1–3):265–79. [3] Hotz C, Peerson JM, Brown KH. Suggested lower cutoffs of serum zinc concentrations for assessing zinc status: reanalysis of the second National Health and Nutrition Examination Survey data. Am J Clin Nutr 2003;78:756–64. [4] Tiran B, Lorenz O, Tiran A, Buchinger W, Eber O. Comparison of direct versus indirect determination of zinc concentration in erythrocytes in euthyroid and hyperthyroid subjects. Eur J Clin Chem Clin Biochem 1993;31:239–44. [5] Knaus WA, Wagner DP, Draper EA, Zimmerman JE, Bergner M, Bastos PG, et al. The APACHE III prognostic system. Risk prediction of hospital mortality for critically ill hospitalized adults. Chest 1991;100(6):1619–36. [6] Prasad AS. Zinc in Human Health: Effect of Zinc on Immune Cells. Mol Med 2008;14(May–Jun (5–6)):353–7. [7] Prasad AS, Beck FWJ, Bao B, Snell DC, Steinberg JD, Cardozo LJ. Zinc supplementation decreases incidence of infections in the elderly: Effect of zinc on generation of cytokines and oxidative stress. Am J Clin Nutr 2007;85:837–44. [8] Clermont G, Vergely C, Jazayeri S, Lahet JJ, Goudeau JJ, Lecour S. Systemic Free Radical Activation Is a Major Event Involved In Myocardial Oxidative Stress Related to Cardiopulmonary Bypass. Anesthesiology 2002;96:80–7. [9] Roohani N, Hurrell R, Kelishadi R, Schulin R. Zinc and its importance for human health: An integrative review. J Res Med Sci 2013;18(Feb (2)):144–57. [10] Buxaderas SC, Farre´-Rovira R. Whole blood and serum zinc levels in relation to sex and age. Rev Esp Fisiol 1985;41(Dec (4)):463–70. [11] Linko R, Karlsson S, Pettila¨ V, Varpula T, Okkonen M, et al. Serum zinc in critically ill adult patients with acute respiratory failure. Acta Anaesthesiol Scand 2011;55(May (5)):615–21. [12] Braun LA, Rosenfeldt F. Pharmaco-nutrient interactions: – a systematic review of zinc and antihypertensive therapy. Int J Clin Pract 2013;67 (August (8)):717–25. [13] Koren-Michowitz M, Dishy V, Zaidenstein R, Yona O, Berman S, Weissgarten J, et al. The effect of losartan and losartan/hydrochlorothiazide fixed-combination on magnesium, zinc, and nitric oxide metabolism in hypertensive patients: a prospective open-label study. Am J Hypertens 2005;18(3):358–63. [14] Garcı´a OP, Ronquillo D, Caaman˜o M, Camacho M, Long KZ, Rosado JL. Zinc, vitamin A, and vitamin C status are associated with leptin concentrations and obesity in Mexican women: results from a cross-sectional study. Nutr Metab 2012;9:59.
Please cite this article in press as: Braun LA, et al. Prevalence of Zinc Deficiency in Cardiac Surgery Patients. Heart, Lung and Circulation (2017), http://dx.doi.org/10.1016/j.hlc.2017.07.009