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Trace elements in hemodialysis patients: a systematic review and meta-analysis

The Alberta Kidney Disease Network, Marcello Tonelli, Natasha Wiebe and 6 more

BMC Medicine · 2009 · Meta-analysis

doi:10.1186/1741-7015-7-25

Abstract

Background. Hemodialysis patients are at risk for deficiency of essential trace elements and excess of toxic trace elements, both of which can affect health. We conducted a systematic review to summarize existing literature on trace element status in hemodialysis patients.

Methods. All studies which reported relevant data for chronic hemodialysis patients and a healthy control population were eligible, regardless of language or publication status. We included studies which measured at least one of the following elements in whole blood, serum, or plasma: antimony, arsenic, boron, cadmium, chromium, cobalt, copper, fluorine, iodine, lead, manganese, mercury, molybdenum, nickel, selenium, tellurium, thallium, vanadium, and zinc. We calculated differences between hemodialysis patients and controls using the differences in mean trace element level, divided by the pooled standard deviation.

Results. We identified 128 eligible studies. Available data suggested that levels of cadmium, chromium, copper, lead, and vanadium were higher and that levels of selenium, zinc and manganese were lower in hemodialysis patients, compared with controls. Pooled standard mean differences exceeded 0.8 standard deviation units (a large difference) higher than controls for cadmium, chromium, vanadium, and lower than controls for selenium, zinc, and manganese. No studies reported data on antimony, iodine, tellurium, and thallium concentrations.

Conclusion. Average blood levels of biologically important trace elements were substantially different in hemodialysis patients, compared with healthy controls. Since both deficiency and excess of trace elements are potentially harmful yet amenable to therapy, the hypothesis that trace element status influences the risk of adverse clinical outcomes is worthy of investigation.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 20, 2026. Paragraph numbers are ours, so an answer can point at one.

Background

Hemodialysis is the most common form of treatment for end-stage renal disease (ESRD), and is associated with considerable morbidity and mortality due to accelerated cardiovascular disease and infection. Despite the well-documented burden of disease, much remains to be learned about how best to prevent these complications of hemodialysis.

Hemodialysis removes uremic toxins primarily by allowing equilibration of plasma and dialysate across a semi-permeable membrane. Dialysate is created by adding carefully regulated quantities of biologically essential ions such as potassium, sodium, bicarbonate, and calcium to water that has been treated to reduce solutes to very low levels. The dialysate concentration of other substances such as trace elements is not routinely manipulated. Substances that have lower concentrations in dialysate than in blood tend to be removed by dialysis. Although this is appropriate in the case of uremic toxins, it may lead to depletion of biologically essential substances. Besides the potential for ongoing removal of trace elements by dialysis, hemodialysis patients are at risk for low dietary intake of such substances due to uremia-related anorexia and dietary restrictions.

Hemodialysis patients are exposed to very high volumes (>300 liters/week) of dialysate. Therefore, even minute levels of toxic substances in source water could lead to tiny concentration gradients between blood and dialysate, which in turn could lead to clinically relevant toxicity. Substances present in dialysate but not in blood will tend to accumulate in the patient, and the lack of renal clearance in hemodialysis patients might theoretically lead to toxicity of ingested trace elements even when they are not present in dialysate. Thus, hemodialysis patients are at theoretical risk for both deficiency and accumulation of trace elements, depending on dietary intake, removal by dialysis, the composition of the source water used for hemodialysis, and residual kidney function.

Deficiency of essential trace elements (such as zinc or selenium) and excess of potentially harmful trace elements (such as lead or arsenic) are both known to have adverse consequences in the general population. Although not established, it is plausible that disordered trace element nutritional status (if present) would contribute to morbidity and mortality among hemodialysis patients as well. However, the incidence of abnormal trace element status in dialysis patients has not been comprehensively studied. We performed a systematic review to compare trace element status between hemodialysis patients and healthy controls.

Data sources and searches

This systematic review is reported according to published guidelines. An expert librarian conducted a comprehensive search to identify all relevant studies regardless of language or publication status. Three electronic databases, MEDLINE (1966 to 13 April 2008), EMBASE (1988 to 13 April 2008), and the Cochrane Library (13 April 2008) were searched. The detailed search strategies are included in Additional file 1. A subject specialist and a methodologist screened each citation or abstract. Any study considered potentially relevant by at least one reviewer was retrieved for further review.

Study selection

The full text of each potentially relevant study was independently assessed by two reviewers for inclusion in the review using predetermined eligibility criteria on a pre-printed form. Studies were eligible for inclusion if they measured trace element concentrations in both a chronic hemodialysis population and a healthy control population. We selected the following trace elements for study a priori based on their known or suspected potential to influence health, and after consideration of existing standards for hemodialysis water quality: antimony, arsenic, boron, cadmium, chromium, cobalt, copper, fluorine, iodine, lead, manganese, mercury, molybdenum, nickel, selenium, tellurium, thallium, vanadium, and zinc. Only studies that measured trace element status in whole blood, serum, or plasma were included. Disagreements were resolved by discussion and consultation with a third party. Disagreements arose with 6% of the articles (κ = 0.88).

Data extraction and quality assessment

We assessed and reported the study quality of included studies using the Downs and Black checklist. Two reviewers independently assessed each included study, and resolved disagreements with the aid of a third party through consensus. An average of 18% of disagreements on quality items occurred. Study characteristics and data of interest were pre-specified, and were recorded in a purpose-built database. One reviewer extracted the data. A second reviewer checked the data for accuracy.

Data synthesis and analysis

We analyzed data using Review Manager 4.2.10 (Oxford, UK) and Stata 10.0 (College Station, Texas, USA). We calculated standardized mean differences (SMD); the hemodialysis population mean minus the control population mean divided by their pooled standard deviation (SD). By presenting the differences in means relative to variability, we removed the heterogeneous effects of both unit and assay, with SMD of 0.2, 0.5, and 0.8 units of SD representing small, medium, and large sizes of effect, respectively. One study reported geometric means rather than arithmetic means, requiring us to standardize the differences in log means rather than the differences in mean.

We assessed heterogeneity using the I2 statistic, and found considerable between-study heterogeneity (I2 >85%). Therefore, the primary method of pooling data across studies used a qualitative approach (vote counting; used to tally the number of studies finding that the level of a particular trace element was lower or higher in hemodialysis patients than in controls). We used the sign test to determine whether the vote count tally was statistically significant (provided that there were at least three studies which reported results for the element in question). To provide guidance on the relative magnitude of the differences between hemodialysis patients and controls, we also report random-effects estimates of the pooled SMD for elements where the sign test indicated that levels were significantly different between these two populations. Given the presence of large heterogeneity, we did not formally assess for the presence of publication bias.

Statistical sources of heterogeneity were explored using weighted least squares meta-regression. The following study-level variables were considered: sample source (whole blood, serum, plasma), mean duration of hemodialysis treatment (in months), continent on which the study was performed (Americas/Europe versus other) and measurement technique (absorption spectroscopy versus other). The effect of sample size was also explored given the tendency for SDs to be underestimated, and therefore SMDs overestimated, when sample sizes are small (N <30).

Search yield

From 1,481 identified citations and abstracts, 226 full articles were retrieved for detailed evaluation (Figure 1). Of these, 128 studies reported relevant data and were included in this review. Most studies were conducted in Europe (47%), Asia (30%), and North America (14%). Seventy-four percent of data came from cross-sectional studies; the remaining data from baseline assessments of randomized controlled trials and prospective cohort studies. Most studies used absorption spectroscopy, emission spectroscopy or neutron activation to measure trace element levels in biological specimens (Additional file 2). Multiple variants of absorption spectroscopy were used.

Populations studied

Sample sizes of hemodialysis patients ranged from 6 to 456 (median 24; Additional file 2). Mean ages ranged from 32 to 74 and percent male ranged from 0% to 100%. Little information was reported on the primary cause of ESRD, co-morbidities, or membrane properties. Control group sample sizes ranged from 5 to 490 (median 28). Mean ages ranged from 28 to 74 and percent male ranged from 0% to 100%. Hospital or laboratory staff (13%), blood donors (7%), non-renal patients (6%), or people drawn from the general population in the same geographic region (6%) were the most commonly specified source populations for control groups. Results of quality assessment are reported in Additional file 2. Time spent on dialysis (39%), description of control participants (29%), and eligibility criteria (20%) were poorly reported. Adjustment or matching for age and sex was infrequent (20%). Technique was well reported (98%), but consideration for measurement error was poor (34%).

Trace element status

Data were available for arsenic, boron, cadmium, chromium, cobalt, copper, fluorine, lead manganese, mercury, molybdenum, nickel, selenium, vanadium, and zinc. The pooled results comparing trace element status for hemodialysis patients with controls are presented in Table 1 and Figure 2. Results stratified by sample source (whole blood, serum, or plasma), or repeated using a fixed-effect model were consistent (data not shown). Available data suggested that levels of cadmium, chromium, copper, lead, and vanadium were higher and that levels of manganese, selenium, and zinc were lower in hemodialysis patients, compared with controls (Table 2). The magnitude of these differences was large (>0.8 SD units) for cadmium, chromium, vanadium, selenium, zinc, and manganese.

Available data for arsenic, boron, cobalt, fluorine, mercury, molybdenum, and nickel were either too limited or too heterogeneous to report. No studies reported data on antimony, fluorine, iodine, tellurium, and thallium.

Meta-regression

We attempted to identify potential explanations for the observed between-study heterogeneity using meta-regression. None of the characteristics considered (sample source, duration of hemodialysis treatment, continent on which the study was performed, or measurement technique) significantly modified the association between hemodialysis treatment and the blood levels of the trace elements studied (data not shown).

Discussion

We found that hemodialysis patients appear to have lower levels of zinc and selenium than people in the general population. Zinc deficiency is a leading cause of disease in developing countries, and is associated with delayed wound healing, and immune deficiency characterized by impaired cell proliferation, abnormal T-cell function, defective phagocytosis, and abnormal cytokine expression, all of which might contribute to the excess risk of infection observed in hemodialysis patients. Zinc deficiency may also cause or contribute to a number of relatively non-specific conditions commonly observed in hemodialysis patients, including anorexia, dysgeusia, and impaired cognitive function.

Although the biological significance of low blood selenium concentrations is less clear, severe selenium deficiency leads to sudden death and cardiomyopathy in the general population. Lower levels of serum selenium without severe deficiency have been associated with hypertension, heart failure, and coronary disease in the general population, and with cardiomyopathy among dialysis patients. Finally, mild selenium deficiency appears to increase susceptibility to oxidant stress, which may be relevant to hemodialysis patients in whom oxidative stress is markedly increased.

In addition to the lower levels of selenium and zinc, hemodialysis patients seem to have higher average levels of certain trace elements compared with healthy controls. It was not possible to compare absolute levels of trace elements across studies (given the different techniques and specimens), and therefore we could not estimate the proportion of hemodialysis patients who have trace element levels in the toxic range. However, for many of the elements, the SMD for the differences between hemodialysis patients and controls exceeded 0.8 SD, which is considered to be a large between-group effect by authorities.

For most of the trace elements studied, the biological significance of higher blood levels is unclear. However, excessive levels of lead or arsenic in blood and other tissues are known to be potentially harmful. For example, minor elevations in whole blood lead levels are associated with impaired cognitive function, impaired hemoglobin synthesis, and hypertension. Cerebrovascular disease and renal insufficiency also appear to be more frequent at higher levels of blood lead, perhaps mediated by higher blood pressure. Thus, higher blood levels of lead may increase the risk of cardiovascular disease, although the mechanism remains unclear. Similarly, inorganic arsenic causes tissue damage by multiple mechanisms including oxidative injury, inhibition of DNA repair, and chromosomal damage (deletion, aneuploidy), and higher levels of arsenic are associated with increased risk of peripheral vascular disease. Animal studies suggest that low selenium status may predispose to arsenic toxicity, and underweight or malnourished humans may also be at increased risk, suggesting that hemodialysis patients may be at higher than average risk of arsenic toxicity.

Implications of the findings

Although the concentration of some trace elements in hemodialysis source water is monitored annually in accordance with federal regulation, blood or body levels of these substances are rarely (if ever) measured in hemodialysis patients. The potential for the accumulation of trace elements to cause harm in hemodialysis patients is exemplified by aluminum. Aluminum toxicity led to serious toxicity (anemia, disabling encephalopathy, neuropathy and severe symptomatic bone disease) in dialysis patients prior to the recognition that aluminum in dialysate and oral medications was responsible. It is difficult to overstate the importance of this discovery for nephrology practice, which led to the elimination of aluminum-related toxicity (and substantial improvements in patient outcomes) within a few years. Today, clinically obvious toxicity due to accumulation of aluminum is exceedingly rare in hemodialysis patients, and the existing regulation has been remarkably effective at reducing the risk of acute toxicity from excess trace elements such as fluorine. However, the possibility that other trace elements may accumulate in patients with kidney failure and cause unrecognized chronic toxicity has received surprisingly little attention.

Oral trace element supplements are readily available, and oral zinc and selenium preparations have been shown to increase blood levels of these elements in dialysis patients. However, few data describe the impact of trace element supplementation on clinical outcomes in hemodialysis patients, despite the fact that correction of zinc deficiency is beneficial in the general population, including significantly reducing the risk of infection and all-cause death. Data examining the relation between trace element status and clinical outcomes in hemodialysis patients are similarly scarce. One relatively small (N = 265) study published in the Lithuanian language shows a significant association between lower plasma zinc levels and the risk of infection. Our data suggest that future studies should investigate the link between zinc or selenium status and clinical outcomes in dialysis patients, in whom the risk of infection is dramatically elevated compared with people with normal kidney function.

Limitations

The available literature has several potentially important limitations. First, study quality was moderate to poor, and many of the studies were relatively small. Second, the available data include multiple different analytical techniques, study populations, control groups, and specimen types (whole blood, serum, plasma). Perhaps for this reason, there was substantial between-study heterogeneity in the results, meaning that the extent to which trace element levels are higher or lower in hemodialysis patients cannot be estimated with certainty. We were unable to identify statistical sources of this heterogeneity, perhaps because we only had access to study-level (rather than patient-level) data. Despite the heterogeneity, for several of the elements studied, the great majority of studies found differences between hemodialysis patients and controls. Since the same technique and specimen types were used for both patients and controls, it is unlikely that these differences are spurious. However, it remains possible that important differences exist for other substances known or suspected to influence health. Third, studies generally did not report data on dietary intake of trace elements and thus we cannot assess whether reduced consumption of foods containing zinc and selenium was responsible for the lower levels of these elements among hemodialysis patients. Fourth, although we found large differences between the blood levels of certain trace elements in hemodialysis patients and those in control participants, the clinical significance of this finding remains to be confirmed. Fifth, although we studied blood levels of trace elements, it is possible that bone or other compartments may better reflect trace element body status, especially for heavy metals such as lead. Sixth, although simultaneous derangement of multiple trace elements (for example, low selenium and excess arsenic) may have synergistic toxicity, the nature of the available data precluded us from determining how frequently this occurs in hemodialysis patients. Finally, although all systematic reviews have potential limitations, we conducted and reported this analysis according to published guidelines aimed at reducing bias. Nonetheless, as with all systematic reviews, the strength of our conclusions is influenced by the quality of the studies on which they are based.

Conclusion

In summary, we found that average blood concentrations of biologically important trace elements were substantially different in hemodialysis patients, compared with healthy controls. Since both deficiency and excess of trace elements are potentially amenable to therapy, the hypothesis that trace element status influences the risk of adverse clinical outcomes appears worthy of investigation, especially when one considers the experience of the nephrology community with aluminum.

Abbreviations

ESRD: end-stage renal disease; SD: standard deviation; SMD: standard mean differences

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

MT contributed to the conception and design, study selection, interpretation of data, and drafted the manuscript. NW managed the project, contributed to the conception and design, managed the acquisition of data (study selection, quality assessment, data extraction), conducted the analysis, and contributed to the drafting of the manuscript. BH, SK, CF, BM, RT, and JG contributed to the conception and design, interpretation of data, and revised the manuscript critically for important intellectual content. All authors approved the final manuscript.

Pre-publication history

The pre-publication history for this paper can be accessed here:

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    Hwang SJ, Chang JM, Lee SC, Tsai JH, Lai YH. Short- and long-term uses of calcium acetate do not change hair and serum zinc concentrations in hemodialysis patients. Scand J Clin Lab Invest. 1999;59:83-87.

    Not in our library10.1080/00365519950185797

  54. 54.

    Bonforte G, Surian M, Dozio B, Scanziani R, Baj A, Colombo S, Toffoletto F. Plasma or whole blood concentrations of trace elements in patients treated by haemodiafiltration with on-line prepared substitution fluid. Nephrol Dial Transplant. 1998;13:29-33.

    Not in our library10.1093/ndt/13.suppl_5.29

  55. 55.

    Chataut CP, Rahman M, Rashid HU, Akhter S, Islam S, Alam M, Ali MS. Serum levels of zinc, copper and magnesium in end stage renal disease subjects and their clinical and biochemical correlations. Bangladesh Renal J. 1998;17:4-9.

    Not in our library

  56. 56.

    Nordio M, Andriani M, Gerotto M, Marchini P, Zambenedetti P, Zatta P. Serum concentration of trace elements during different stages of chronic renal failure. Ital J Miner Elect M. 1998;12:81-86.

    Not in our library

  57. 57.

    Turk S, Bozfakioglu S, Ecder ST, Kahraman T, Gurel N, Erkoc R, Aysuna N, Turkmen A, Bekiroglu N, Ark E. Effects of zinc supplementation on the immune system and on antibody response to multivalent influenza vaccine in hemodialysis patients. Int J Artif Organs. 1998;21:274-278.

    Not in our library

  58. 58.

    Zhang X, Cornelis R, Mees L, Vanholder R, Lameire N. Chemical speciation of arsenic in serum of uraemic patients. Analyst. 1998;123:13-17.

    Not in our library10.1039/a704841f

  59. 59.

    Zima T, Mestek O, Tesar V, Tesarova P, Nemecek K, Zak A, Zeman M. Chromium levels in patients with internal diseases. Biochem Mol Biol Int. 1998;46:365-374.

    Not in our library10.1080/15216549800203872

  60. 60.

    Hung KY, Ho CY, Kuo YM, Lee SH, Hseih SJ, Yang CS, Peng CJ, Wu DJ, Hung JT, Chen PY, et al. Trace elements burden in geriatric hemodialysis patients: a prospective multicenter collaborative study. Int J Artif Organs. 1997;20:553-556.

    Not in our library

  61. 61.

    Iotova P, Ionova D, Kuleva V, Antonov S, Tzachev K, Nachev C. Zinc in plasma and platelets in patients on regular haemodialysis. Nephrol Dial Transplant. 1997;12:370-371.

    Not in our library10.1093/ndt/12.2.370

  62. 62.

    Koenig JS, Fischer M, Bulant E, Tiran B, Elmadfa I, Druml W. Antioxidant status in patients on chronic hemodialysis therapy: impact of parenteral selenium supplementation. Wien Klin Wochenschr. 1997;109:13-19.

    Not in our library

  63. 63.

    Bonomini M, Forster S, Manfrini V, De Risio F, Steiner M, Vidovich MI, Klinkmann H, Ivanovich P, Albertazzi A. Geographic factors and plasma selenium in uremia and dialysis. Nephron. 1996;72:197-204.

    Not in our library10.1159/000188842

  64. 64.

    Emenaker NJ, DiSilvestro RA, Nahman NS, Percival S. Copper-related blood indexes in kidney dialysis patients. Am J Clin Nutr. 1996;64:757-760.

    Not in our library10.1093/ajcn/64.5.757

  65. 65.

    Gunduz Z, Dusunsel R, Kose K, Utas C, Dogan P. The effects of dialyzer reuse on plasma antioxidative mechanisms in patients on regular hemodialysis treatment. Free Radic Biol Med. 1996;21:225-231.

    Not in our library10.1016/0891-5849(96)00021-4

  66. 66.

    Lin TH, Chen JG, Liaw JM, Juang JG. Trace elements and lipid peroxidation in uremic patients on hemodialysis. Biol Trace Elem Res. 1996;51:277-283.

    Not in our library10.1007/bf02784082

  67. 67.

    Marchante-Gayon JM, Sanchez-Uria JE, Sanz-Medel A. Serum and tissue selenium contents related to renal disease and colon cancer as determined by electrothermal atomic absorption spectrometry. J Trace Elem Med Biol. 1996;10:229-236.

    Not in our library10.1016/s0946-672x(96)80040-x

  68. 68.

    Rashid HU, Khan AH, Sarker MH, Akhter S, Khan MF. Effect of haemodialysis on serum zinc, copper and magnesium levels in patients with end stage renal failure. Bangladesh Renal J. 1996;15:15-17.

    Not in our library

  69. 69.

    Romero RA, Salgado O, Rodriguez-Iturbe B, Tahan JE. Blood levels of chromium in diabetic and nondiabetic hemodialysis patients. Transplant Proc. 1996;28:3382-3384.

    Not in our library

  70. 70.

    Yoshimura S, Suemizu H, Nomoto Y, Sakai H, Katsuoka Y, Kawamura N, Moriuchi T. Plasma glutathione peroxidase deficiency caused by renal dysfunction. Nephron. 1996;73:207-211.

    Not in our library10.1159/000189042

  71. 71.

    Bonomini M, Manfrini V, Marini A, De Risio F, Niri L, Klinkmann H, Albertazzi A. Hemodialysis with regenerated cellulosic membranes does not reduce plasma selenium levels in chronic uremic patients. Artif Organs. 1995;19:81-85.

    Not in our library10.1111/j.1525-1594.1995.tb02249.x

  72. 72.

    Granadillo VA, Salgado O, Barrios Ch L, Romero RA. Distribution of chromium in blood components of diabetics and azotemic patients. Trace Elem Electroly. 1995;12:76-80.

    Not in our library

  73. 73.

    Granadillo VA, Tahan JE, Salgado O, Elejalde LE, Rodriguez-Iturbe B, Romero GB, Romero RA. The influence of the blood levels of lead, aluminum and vanadium upon the arterial hypertension. Clin Chim Acta. 1995;233:47-59.

    Not in our library10.1016/0009-8981(94)05966-v

  74. 74.

    Cheng PL, Wang Hsu GS. The zinc status in uremic patients with or without hemodialysis. J Chin Nutr Soc. 1994;19:151-157.

    Not in our library

  75. 75.

    Hasanoglu E, Altan N, Sindel S, Ongun CO, Bali M, Altintas E. The relationship between erythrocyte superoxide dismutase activity and plasma levels of some trace elements (Al, Cu, Zn) of dialysis patients. Gen Pharmacol. 1994;25:107-110.

    Not in our library10.1016/0306-3623(94)90018-3

  76. 76.

    Loughrey CM, Young IS, Lightbody JH, McMaster D, McNamee PT, Trimble ER. Oxidative stress in haemodialysis. QJM. 1994;87:679-683.

    Not in our library

  77. 77.

    Antos M, Jeren-Strujic B, Romic Z, Matanovic B, Gudel-Greguric J. Serum selenium levels in patients on hemodialysis. Trace Elem Med. 1993;10:173-176.

    Not in our library

  78. 78.

    Colleoni N, Arrigo G, Gandini E, Corigliano C, D'Amico G. Blood lead in hemodialysis patients. Am J Nephrol. 1993;13:198-202.

    Not in our library10.1159/000168618

  79. 79.

    De Kimpe J, Cornelis R, Mees L, Van Lierde S, Vanholder R. More than tenfold increase of arsenic in serum and packed cells of chronic hemodialysis patients. Am J Nephrol. 1993;13:429-434.

    Not in our library10.1159/000168658

  80. 80.

    Girelli D, Olivieri O, Stanzial AM, Azzini M, Lupo A, Bernich P, Menini C, Gammaro L, Corrocher R. Low platelet glutathione peroxidase activity and serum selenium concentration in patients with chronic renal failure: relations to dialysis treatments, diet and cardiovascular complications. Clin Sci (Colch). 1993;84:611-617.

    Not in our library10.1042/cs0840611

  81. 81.

    Holtkamp W, Brodersen HP, Stollberg T, Thiery J, Falkner C. Zinc supplementation stimulates tetanus antibody formation and soluble interleukin-2 receptor levels in chronic hemodialysis patients. Clin Investig. 1993;71:537-541.

    Not in our library10.1007/bf00208476

  82. 82.

    Hosokawa S, Yoshida O. Effects of erythropoietin on trace elements in patients with chronic renal failure undergoing hemodialysis. Nephron. 1993;65:414-417.

    Not in our library10.1159/000187522

  83. 83.

    Mayer DR, Kosmus W, Pogglitsch H, Mayer D, Beyer W. Essential trace elements in humans. Serum arsenic concentrations in hemodialysis patients in comparison to healthy controls. Biol Trace Elem Res. 1993;37:27-38.

    Not in our library10.1007/bf02789399

  84. 84.

    Shu KH, Lu YS, Chen CH, Chen DC, Lee SH, Lian JD. Lymphocyte proliferation in uremic patients: correlation with zinc status. J Formos Med Assoc. 1993;92:1017-1020.

    Not in our library

  85. 85.

    Mihailovic M, Lindberg P, Jovanovic I, Antic D. Selenium status of patients with Balkan endemic nephropathy. Biol Trace Elem Res. 1992;33:71-77.

    Not in our library10.1007/bf02783994

  86. 86.

    Milly K, Wit L, Diskin C, Tulley R. Selenium in renal failure patients. Nephron. 1992;61:139-144.

    Not in our library10.1159/000186861

  87. 87.

    Navarro JA, Granadillo VA, Salgado O, Rodriguez-Iturbe B, Garcia R, Delling G, Romero RA. Bone metal content in patients with chronic renal failure. Clin Chim Acta. 1992;211:133-142.

    Not in our library10.1016/0009-8981(92)90189-w

  88. 88.

    Turan B, Delilbasi E, Dalay N, Sert S, Afrasyap L, Sayal A. Serum selenium and glutathione-peroxidase activities and their interaction with toxic metals in dialysis and renal transplantation patients. Biol Trace Elem Res. 1992;33:95-102.

    Not in our library10.1007/bf02783997

  89. 89.

    Kouw PM, Konings CH, de Vries PM, Meulen J van der, Oe PL. Effects of zinc supplementation on zinc status and immunity in haemodialysis patients. J Trace Elem Elect H. 1991;5:115-119.

    Not in our library

  90. 90.

    Richard MJ, Arnaud J, Jurkovitz C, Hachache T, Meftahi H, Laporte F, Foret M, Favier A, Cordonnier D. Trace elements and lipid peroxidation abnormalities in patients with chronic renal failure. Nephron. 1991;57:10-15.

    Not in our library10.1159/000186208

  91. 91.

    Clyne N, Lins LE, Pehrsson SK. Serum cobalt in relation to residual renal function in uremic patients before and after renal transplantation. Trace Elem Med. 1990;7:173-175.

    Not in our library

  92. 92.

    Kostakopoulos A, Kotsalos A, Alexopoulos J, Sofras F, Deliveliotis C, Kallistratos G. Serum selenium levels in healthy adults and its changes in chronic renal failure. Int Urol Nephrol. 1990;22:397-401.

    Not in our library10.1007/bf02549802

  93. 93.

    Romero RA, Navarro JA, Rodriguez-Iturbe B, Parra OE, Granadillo VA. Distribution of trace metals in blood components of patients with chronic renal failure undergoing periodical hemodialysis treatment. Trace Elem Med. 1990;7:176-181.

    Not in our library

  94. 94.

    Togni E, Travaglini P, Beretta C, Berardinelli L, Vegeto A, Mocchegiani E, Fabris N, Egidi F, Ponticelli C, Faglia G. Prolactin, thymulin and zinc in chronic hemodialysis: effect of renal transplant. J Endocrinol Invest. 1990;13:709-715.

    Not in our library10.1007/bf03349606

  95. 95.

    Tsukamoto Y, Saka S, Kumano K, Iwanami S, Ishida O, Marumo F. Abnormal accumulation of vanadium in patients on chronic hemodialysis therapy. Nephron. 1990;56:368-373.

    Not in our library10.1159/000186177

  96. 96.

    Agenet C, Brugere CC, Reynier JP. Plasma and intra-erythrocytic concentrations of copper and zinc in uremic patients treated by periodic hemodialysis. Ann Biol Clin (Paris). 1989;47:493-496.

    Not in our library

  97. 97.

    Hachache T, Meftahi H, Foret M, Kuentz F, Milongo R, Christollet M, Cordonnier DJ, Arnaud J, Favier A. Short- (1 session) and long-term (6 months) course of the serum level of zinc in 33 hemodialysis patients. Nephrologie. 1989;10:87-90.

    Not in our library

  98. 98.

    Hopfer SM, Fay WP, Sunderman FW. Serum nickel concentrations in hemodialysis patients with environmental exposure. Ann Clin Lab Sci. 1989;19:161-167.

    Not in our library

  99. 99.

    Ishida O, Kihira K, Tsukamoto Y, Marumo F. Improved determination of vanadium in biological fluids by electrothermal atomic absorption spectrometry. Clin Chem. 1989;35:127-130.

    Not in our library

  100. 100.

    Mahajan SK, Bowersox EM, Rye DL, Abu-Hamdan DK, Prasad AS, McDonald FD, Biersack KL. Factors underlying abnormal zinc metabolism in uremia. Kidney Int Suppl. 1989;27:S269-S273.

    Not in our library

  101. 101.

    Navarro J, Parra O, Garcia R, Rodriguez-Iturbe B, Granadillo V, Rubio P, Romero R. Trace metal levels during hemodialysis in patients with chronic renal failure. Trace Elem Med. 1989;6:70-74.

    Not in our library

  102. 102.

    Nixon DE, Moyer TP, Squillace DP, McCarthy JT. Determination of serum nickel by graphite furnace atomic absorption spectrometry with Zeeman-effect background correction: values in a normal population and a population undergoing dialysis. Analyst. 1989;114:1671-1674.

    Not in our library10.1039/an9891401671

  103. 103.

    Saint-Georges MD, Bonnefont DJ, Bourely BA, Jaudon MC, Cereze P, Chaumeil P, Gard C, D'Auzac CL. Correction of selenium deficiency in hemodialyzed patients. Kidney Int Suppl. 1989;27:S274-S277.

    Not in our library

  104. 104.

    Sampson B, Curtis JR, Davies S. Survey of blood lead and plasma aluminium concentrations in patients of a renal unit. Nephrol Dial Transplant. 1989;4:375-381.

    Not in our library10.1093/oxfordjournals.ndt.a091893

  105. 105.

    Travaglini P, Moriondo P, Togni E, Venegoni P, Bochicchio D, Conti A, Ambroso G, Ponticelli C, Mocchegiani E, Fabris N, et al. Effect of oral zinc administration on prolactin and thymulin circulating levels in patients with chronic renal failure. J Clin Endocrinol Metab. 1989;68:186-190.

    Not in our library10.1210/jcem-68-1-186

  106. 106.

    Abu-Hamdan DK, Mahajan SK, Migdal S, Prasad AS, McDonald FD. Zinc tolerance test in uremia: effect of calcitriol supplementation. J Am Coll Nutr. 1988;7:235-240.

    Not in our library10.1080/07315724.1988.10720240

  107. 107.

    Foote JW, Hinks LJ. Zinc absorption in haemodialysis patients [see comment]. Ann Clin Biochem. 1988;25:398-402.

    Not in our library10.1177/000456328802500413

  108. 108.

    Kuroda M, Imura T, Morikawa K, Hasegawa T. Decreased serum levels of selenium and glutathione peroxidase activity associated with aging, malignancy and chronic hemodialysis. Trace Elem Med. 1988;5:97-103.

    Not in our library

  109. 109.

    Mendes V, Romao Junior JE, Kirschbaum E, Andriollo A, Marcondes M, Sabbaga E. Serum zinc in patients undergoing chronic hemodialysis. Rev Hosp Clin Fac Med Sao Paulo. 1988;43:225-227.

    Not in our library

  110. 110.

    Sondheimer JH, Mahajan SK, Rye DL, Abu-Hamdan DK, Migdal SD, Prasad AS, McDonald FD. Elevated plasma copper in chronic renal failure. Am J Clin Nutr. 1988;47:896-899.

    Not in our library10.1093/ajcn/47.5.896

  111. 111.

    Chen HJ, Lai YH, Lin SM, Tsai JH. Taste acuity and zinc in uremic patients undergoing long-term hemodialysis. Taiwan I Hsueh Hui Tsa Chih. 1987;86:158-163.

    Not in our library

  112. 112.

    Dworkin B, Weseley S, Rosenthal WS, Schwartz EM, Weiss L. Diminished blood selenium levels in renal failure patients on dialysis: correlations with nutritional status. Am J Med Sci. 1987;293:6-12.

    Not in our library10.1097/00000441-198701000-00003

  113. 113.

    Foote JW, Hinks LJ. Reduced leucocyte zinc and albumin-bound zinc in blood of haemodialysis patients. Ann Clin Biochem. 1987;24:198-202.

    Not in our library10.1177/000456328702400214

  114. 114.

    Foote JW, Hinks LJ, Lloyd B. Reduced plasma and white blood cell selenium levels in haemodialysis patients. Clin Chim Acta. 1987;164:323-328.

    Not in our library10.1016/0009-8981(87)90307-x

  115. 115.

    Hosokawa S, Nishitani H, Umemura K, Tomoyoshi T, Sawanishi K, Yoshida O. Serum and corpuscular nickel and zinc in chronic hemodialysis patients. Nephron. 1987;45:151-153.

    Not in our library10.1159/000184098

  116. 116.

    Ruiz Alcantarilla P, Lozano Diaz A, Gomez Rodriguez F. Plasma zinc levels, nutritional status and immune response in chronic renal insufficiency. Rev Clin Esp. 1987;181:142-145.

    Not in our library

  117. 117.

    Sanada S, Kuze M, Yoshida O. Beneficial effect of zinc supplementation on pruritus in hemodialysis patients with special reference to changes in serum histamine levels. Hinyokika Kiyo. 1987;33:1955-1960.

    Not in our library

  118. 118.

    Shu KH, Lian JD, Yang YF, Lu YS, Cheng CH, Chen DL. Plasma zinc level in hemodialysis, continuous ambulatory peritoneal dialysis and renal transplantation. Taiwan I Hsueh Hui Tsa Chih. 1987;86:1251-1255.

    Not in our library

  119. 119.

    Abu-Hamdan DK, Mahajan SK, Migdal SD, Prasad AS, McDonald FD. Zinc tolerance test in uremia. Effect of ferrous sulfate and aluminum hydroxide. Ann Intern Med. 1986;104:50-52.

    Not in our library10.7326/0003-4819-104-1-50

  120. 120.

    Chen HJ, Lai YH, Lin SM, Tsai JH. Serum copper and effect of dialysis on it in uremic patients. Taiwan I Hsueh Hui Tsa Chih. 1986;85:539-544.

    Not in our library

  121. 121.

    Hosokawa S, Koike T, Kawaji A, Nishitani H, Nishio T, Tomoyoshi T, Sawanishi K, Yoshida O. Zinc transport during hemodialysis. Artif Organs. 1986;10:30-36.

    Not in our library10.1111/j.1525-1594.1986.tb02513.x

  122. 122.

    Mauras Y, Ang KS, Simon P, Tessier B, Cartier F, Allain P. Increase in blood plasma levels of boron and strontium in hemodialyzed patients. Clin Chim Acta. 1986;156:315-320.

    Not in our library10.1016/0009-8981(86)90074-4

  123. 123.

    Drazniowsky M, Parkinson IS, Ward MK, Channon SM, Kerr DN. Raised serum nickel concentrations in chronic renal failure. Proc Eur Dial Transplant Assoc Eur Ren Assoc. 1985;21:241-246.

    Not in our library

  124. 124.

    Hosokawa S, Nishitani H, Umemura K, Nishio T, Tomoyoshi T, Sawanishi K, Yoshida O. Relationship between haemodialysis anaemia and copper and zinc. Int Urol Nephrol. 1985;17:365-371.

    Not in our library10.1007/bf02083507

  125. 125.

    Hosokawa S, Nishitani H, Tomita K, Tomoyoshi T, Nishio T, Sawanishi K, Yoshida O. Serum copper concentration changes in chronic hemodialyzed patients. Uremia Invest. 1985;9:63-67.

    Not in our library10.3109/08860228509104841

  126. 126.

    Kallistratos G, Evangelou A, Seferiadis K, Vezyraki P, Barboutis K. Selenium and haemodialysis: serum selenium levels in healthy persons, non-cancer and cancer patients with chronic renal failure. Nephron. 1985;41:217-222.

    Not in our library10.1159/000183586

  127. 127.

    Wills MR, Brown CS, Bertholf RL, Ross R, Savory J. Serum and lymphocyte, aluminum and nickel in chronic renal failure. Clin Chim Acta. 1985;145:193-196.

    Not in our library10.1016/0009-8981(85)90286-4

  128. 128.

    Minami T, Samukawa K, Adachi K, Okazaki Y. Change of serum chromium level in chronic hemodialysis patients. Yakugaku Zasshi. 1984;104:816-818.

    Not in our library10.1248/yakushi1947.104.7_816

  129. 129.

    Piechota W, Dobrucki T, Symonowicz N, Wadowska E, Murkowska E. Zinc in patients with chronic renal failure. Int Urol Nephrol. 1983;15:377-382.

    Not in our library10.1007/bf02082558

  130. 130.

    Thomson NM, Stevens BJ, Humphery TJ, Atkins RC. Comparison of trace elements in peritoneal dialysis, hemodialysis, and uremia. Kidney Int. 1983;23:9-14.

    Not in our library10.1038/ki.1983.3

  131. 131.

    Mahajan SK, Prasad AS, Rabbani P, Briggs WA, McDonald FD. Zinc deficiency: a reversible complication of uremia. Am J Clin Nutr. 1982;36:1177-1183.

    Not in our library10.1093/ajcn/36.6.1177

  132. 132.

    Okuyama S, Mishina H, Hasegawa K, Nakano N, Ise K. Probable atherogenic role of zinc and copper as studied in chronic hemodialysis patients. Tohoku J Exp Med. 1982;138:227-229.

    Not in our library10.1620/tjem.138.227

  133. 133.

    Temes-Montes XL, Picaporte MA, Herrero E, Otero A, Sanchez-Guisande D, Sanchez-Sicilia L. Zinc in patients with chronic renal insufficiency subjected to periodic maintenance hemodialysis. Rev Clin Esp. 1982;165:189-191.

    Not in our library

  134. 134.

    Paniagua-Sierra JR, Perez-Lopez A, Diaz-Bensussen S, Solis-Alpuche L, Saavedra-Guatemala H, Exaire-Murad JE. Zinc and copper concentration in plasma and erythrocytes of patients with chronic renal failure. Arch Invest Med (Mex). 1981;12:69-82.

    Not in our library

  135. 135.

    Schiffl HH, Binswanger U. Human urinary fluoride excretion as influenced by renal functional impairment. Nephron. 1980;26:69-72.

    Not in our library10.1159/000181954

  136. 136.

    Tsukamoto Y, Iwanami S, Marumo F. Disturbances of trace element concentrations in plasma of patients with chronic renal failure. Nephron. 1980;26:174-179.

    Not in our library10.1159/000181976

  137. 137.

    Cornelis R, Mees L, Ringoirs S, Hoste J. Serum and red blood cell Zn, Se, Cs and Rb in dialysis patients. Miner Electrolyte Metab. 1979;2:88-93.

    Not in our library

  138. 138.

    Mahajan SK, Prasad AS, Rabbani P, Briggs WA, McDonald FD. Zinc metabolism in uremia. J Lab Clin Med. 1979;94:693-698.

    Not in our library

  139. 139.

    Marumo F, Tsukamoto Y, Iwanami S, Kishimoto T, Yamagami S. Effects of hemofiltration and hemodialysis on contents of trace elements in hair, nails and plasma of patients with chronic renal failure. Proc Clin Dial Transplant Forum. 1979;9:160-164.

    Not in our library

  140. 140.

    Mountokalakis T, Dakanalis D, Boukis D, Virvidakis K, Voudiklari S, Koutselinis A. Hair zinc compared with plasma zinc in uremic patients before and during regular hemodialysis. Clin Nephrol. 1979;12:206-209.

    Not in our library

  141. 141.

    Zumkley H, Bertram HP, Lison A, Knoll O, Losse H. Aluminum, zinc and copper concentrations in plasma in chronic renal insufficiency. Clin Nephrol. 1979;12:18-21.

    Not in our library

  142. 142.

    Mahajan SK, Gardiner WH, Abbasi AA, Briggs WA, Prasad AS, McDonald FD. Abnormal plasma and erythrocyte zinc distribution in uremia. Trans Am Soc Artif Intern Organs. 1978;24:50-54.

    Not in our library

  143. 143.

    Willden EG, Hyne BE. Blood and urinary cadmium in chronic renal failure. Nephron. 1974;13:253-257.

    Not in our library10.1159/000180400

  144. 144.

    Rudolph H, Alfrey AC, Smythe WR. Muscle and serum trace element profile in uremia. Trans Am Soc Artif Intern Organs. 1973;19:456-465.

    Not in our library10.1097/00002480-197301900-00079

  145. 145.

    Rose GA, Willden EG. Whole blood, red cell and plasma total and ultrafiltrable zinc levels in normal subjects and patients with chronic renal failure with and without haemodialysis. Br J Urol. 1972;44:281-286.

    Not in our library10.1111/j.1464-410x.1972.tb10077.x

  146. 146.

    Barbour BH, Bischel M, Abrams DE. Copper accumulation in patients undergoing chronic hemodialysis. The role of cuprophan. Nephron. 1971;8:455-462.

    Not in our library10.1159/000179949

  147. 147.

    Mahler DJ, Walsh JR, Haynie GD. Magnesium, zinc, and copper in dialysis patients. Am J Clin Pathol. 1971;56:17-23.

    Not in our library10.1093/ajcp/56.1.17

  148. 148.

    Mansouri K, Halsted JA, Gombos EA. Zinc, copper, magnesium and calcium in dialyzed and nondialyzed uremic patients. Arch Intern Med. 1970;125:88-93.

    Not in our library10.1001/archinte.125.1.88

  149. 149.

    Zazgornik J, Kotzaurek R, Schmidt P. Plasma zinc concentration in uremic patients during hemodialysis. Klin Wochenschr. 1971;49:278-280.

    Not in our library10.1007/bf01485431

  150. 150.

    Rink L, Gabriel P. Zinc and the immune system. Proc Nutr Soc. 2000;59:541-552.

    Not in our library10.1017/s0029665100000781

  151. 151.

    Shankar AH, Prasad AS. Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr. 1998;68:447S-463S.

    Not in our library10.1093/ajcn/68.2.447s

  152. 152.

    Collins AJ, Kasiske B, Herzog C, Chavers B, Foley R, Gilbertson D, Grimm R, Liu J, Louis T, Manning W, Matas A, McBean M, Murray A, St Peter W, Xue J, Fan Q, Guo H, Li S, Roberts T, Snyder J, Solid C, Wang C, Weinhandl E, Arko C, Chen SC, Dalleska F, Daniels F, Dunning S, Ebben J, Frazier E, et al. Excerpts from the United States Renal Data System 2004 annual data report: atlas of end-stage renal disease in the United States. Am J Kidney Dis. 2005;45:A5-7.

    Not in our library10.1053/j.ajkd.2004.10.009

  153. 153.

    Oliver MJ, Rothwell DM, Fung K, Hux JE, Lok CE. Late creation of vascular access for hemodialysis and increased risk of sepsis. J Am Soc Nephrol. 2004;15:1936-1942.

    Not in our library10.1097/01.asn.0000131524.52012.f8

  154. 154.

    Allon M. Dialysis catheter-related bacteremia: treatment and prophylaxis. Am J Kidney Dis. 2004;44:779-791.

    Not in our library10.1016/s0272-6386(04)01078-9

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    Mokrzycki MH, Zhang M, Cohen H, Golestaneh L, Laut JM, Rosenberg SO. Tunnelled haemodialysis catheter bacteraemia: risk factors for bacteraemia recurrence, infectious complications and mortality. Nephrol Dial Transplant. 2006;21:1024-1031.

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    The Epidemiology of Lead Toxicity in Adults: Measuring Dose and Consideration of Other Methodologic Issues · 2006
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