Association of Nutritional Assessment
by Phase Angle With Mortality in Kidney
Transplant Patients in an 8-Year Follow-Up
Eda kaya, MD
1, Alev Bakir, PhD
2, Yusuf Kenan Koseoglu, MD
3,
Mehmet Velidedeoglu, MD
4, Sinan Trabulus, MD
3,
and Nurhan Seyahi, MD
3Abstract
Background: Phase angle is a bioimpedance analysis parameter that indirectly shows body cell mass. Its association with mortality has been shown in patients receiving dialysis treatment. However, assessment with mortality in kidney transplant recipients has not been studied previously. Methods: We examined 158 kidney transplant recipients who underwent bioim-pedance analysis 8 years ago in a cross-sectional study. We contacted them again and investigated the presence of cardiovascular events, cancer, angina pectoris, and claudication. Data regarding mortality, graft failure, and creatinine values were collected from recipients’ files. Findings: During the follow-up period, 15 recipients died, 26 lost graft function, 36 experienced cardiovascular events, and 4 developed cancer. Phase angle was significantly associated with mortality during the 8-year follow-up period of kidney transplant recipients (P < .001). The cutoff value for phase angle as a predictor of mortality was5.85. Moreover, a phase angle value lower than 5.85 indicated 5.33 times higher risk of mortality. Discussion: Phase angle was a predictor of mortality in kidney transplant recipients. Since phase angle is an inexpensive, easy-to-perform, and noninvasive method, it might be considered as an additional tool to assess survival in kidney transplant recipients.
Keywords
kidney transplant recipient, body regions, nutritional and metabolic diseases, population characteristics, health occupations, cardiovascular system
Introduction
Nutritional status is an important clinical assessment in patients with renal diseases, as malnutrition is regularly associated with increased complications, morbidity, and mortality.1,2There are various methods to assess patients’ nutritional status including biochemical and anthropometric indices, immunological tests, and subjective global assessment forms.3
Bioelectrical impedance analysis (BIA) is a practical mea-surement to assess body composition.4 Resistance and reac-tance are BIA-derived parameters that are measured by the BIA device. Resistance predicts patient’s hydration status, and it is associated with the amount of water in the body. Reactance shows the amount of energy that can be accumulated in tissue, which can be considered as a capacitator.5Phase angle is the raw BIA parameter that is directly measured by the bioimpe-dance device and defined as the arctangent of the reactance-to-resistance ratio. It is also an indirect predictor of cell membrane integrity and body cell mass.6It is well known that phase angle is used in the assessment of nutritional status. The lower the phase angle, the worse the nutritional status of the evaluated patient. Furthermore, phase angle provides a more accurate result compared to other BIA-related body composition
estimates because of avoiding estimated calculations such as lean body mass or total body water.7-11
A significant association between a lower phase angle with increased mortality has been shown in previous studies per-formed in elderly populations.8-10Moreover, the association between phase angle and mortality has also been shown in both hemodialysis and peritoneal dialysis patients.11According to the study by Abad et al, lower phase angle was significantly associated with higher mortality rates referring to higher rates of protein calorie malnutrition.11Evaluation of nutritional status
1Cerrahpasa Medical Faculty, Istanbul University-Cerrahpasa, Fatih, Turkey 2Faculty of Medicine, Department of Biostatistics and Medical Informatics,
Halic University, Istanbul, Turkey
3Division of Nephrology, Department of Internal Medicine, Cerrahpasa
Medical Faculty, Istanbul University-Cerrahpasa, Istanbul, Turkey
4
Department of General Surgery, Cerrahpasa Medical Faculty, Istanbul University-Cerrahpasa, Istanbul, Turkey
Corresponding Author:
Nurhan Seyahi, Division of Nephrology, Department of Internal Medicine, Cerrahpasa Medical Faculty, Istanbul University-Cerrahpasa, Halaskargazi Cad. No: 87 Huzur Apt. Sisli, 34360, Istanbul, Turkey.
Email: nseyahi@yahoo.com
2019, Vol. 29(4) 321-326
ª2019, NATCO. All rights reserved. Article reuse guidelines:
sagepub.com/journals-permissions DOI: 10.1177/1526924819873906 journals.sagepub.com/home/pit
in kidney transplant recipients differs between early and late transplantation period. In the early posttransplantation period, the metabolic demand is increased following aggressive immu-nosuppressive treatment to preserve graft function. Therefore, it is important to provide sufficient amount of nutrition in the early transplantation period. In late transplantation period, due to the side effects of immunosuppressive therapy precautions are needed to prevent obesity and related complications.12
To the best of our knowledge, the association of phase angle with mortality in long-term follow-up was not studied previ-ously in kidney transplant recipients in a formal study. In this study, we aimed to investigate the association between phase angle and the mortality in kidney transplant recipients.
Methods
Design, Setting, and Sampling
We performed a cohort study using baseline cross-sectional data from a previously published study.13 In the cross-sectional phase, which represents our population, we collected the baseline data of 158 consecutive kidney transplant recipi-ents between January and October 2010 who were followed up in our outpatient clinic. For that study, adult individuals (18 years of age) who had given informed consent were recruited in the study. Recipients with any of the following conditions were excluded from the study: duration of transplantation less than 1 year, presence of malignancy, or presence of active infection.13 The study protocol was approved by the local medical ethics committee (protocol number: 20546). The study was in adher-ence to the principles of the Declaration of Helsinki.
During 2010, approximately 350 kidney transplant recipients were regularly followed up in our transplantation unit. The unit is located in a tertiary-care center with a yearly transplantation activity of 25 to 30. The frequencies of the regular visits were planned individually according to the recipients’ clinical status. From those, between January and October 2010, we recruited the kidney transplant recipients who showed up for their routine follow-ups and gave informed consent to be included in the study. The immunosuppressive protocol consisted of induction ther-apy with rabbit antithymocyte globulin (in deceased donor trans-plantation) or basiliximab (in immunologically high-risk living transplantation), followed by maintenance therapy with a calci-neurin inhibitor (tacrolimus or cyclosporine), mycophenolate mofetil or mycophenolate sodium, and low-dose prednisolone (5 mg/d). No induction therapy was used in low-risk living donor kidney transplantation. All recipients who had a diagnosis of an acute rejection episode received bolus steroids. Further treat-ment was tailored according to the severity of rejection.
Baseline Data Collection During the Cross-Sectional
Phase (January-October 2010)
Demographic (age and gender), clinical (date of transplanta-tion, donor type, height, and weight), and previous renal
replacement therapy (type and duration) data were collected from the recipients’ files.
The following data were collected using a standardized questionnaire. The date of interview was accepted as the enroll-ment date to the study. The kidney transplant recipients had a clinical and biochemical evaluation. We recorded the antihy-pertensive, antidiabetic, and antilipemic drug use and past his-tory of cardiovascular events (CVE). Cardiovascular events were defined as having had angina pectoris, claudication, or previous history of any cardiovascular disease. Immunosup-pressive medications were also recorded. Physical activity was assessed with the question, “Do you exercise regularly for at least 30 minutes three times per week?” (Response choices: Yes/No). Data on biopsy-proven acute rejection episodes were collected from recipient files. Laboratory tests were performed within 10 days of enrollment with blood samples collected after an overnight fasting period. Albumin, creatinine, low-density lipoprotein, high-density lipoprotein, triglycerides, and fasting blood glucose values were measured. The laboratory para-meters were analyzed using Abbott Architect c8000 autoana-lyzer (Abbott Diagnostics, Abbott Park, Illinois). We calculated glomerular filtration rate (GFR) using Modification of Diet in Renal Disease (MDRD) study equation. Systolic and diastolic blood pressures were measured following a rest period with a semiautomatic device (OMRON M2 Compact HEM-7102-E).
Biometric impedance analysis was performed by a nurse using a single frequency (50 kHz) bioimpedance analyzer (BIA 450; Biodynamics Corp, Shoreline, Washington) during regu-lar follow-ups following an overnight fasting and resting period at a room temperature of 25C. We followed the manufactur-er’s instructions to perform the BIA analysis. The electrodes were placed in the standard tetrapolar positions to the nonac-cess side of the individual. Resistance and reactance were directly measured, and the body fat mass was calculated using the integrated software of the equipment. The reference ranges for BIA parameters calculated according to age and gender were reported before.14
Follow-Up Data Collection for Cohort Study
The recipients were contacted by a physician blinded to the results of BIA who assessed patient for CVE and cancer in March and April 2018. Two standardized questionnaires were used to gather this information. The Rose Questionnaire15was used to assess presence of myocardial infarction (yes/no) and angina pectoris (yes/no) and the Edinburgh Claudication Ques-tionnaire16to assess presence of intermittent claudication (yes/ no). The history of cancer and stroke were gathered with sep-arate questions. The physician marked the responses of the recipients. Serum creatinine values from the last 6 months were recorded form the recipients’ files, and the estimated GFR was calculated according to the MDRD formula. The kidney trans-plant recipients with graft failure were excluded from calcula-tions regarding creatinine and MDRD.
Statistical Analysis
Descriptive statistics were used to describe study sample charac-teristics. Continuous data were expressed as mean (standard deviation) and median [minimum-maximum]. Categorical data were expressed as counts and proportions and were analyzed with the w2or Fisher exact tests. The independent samples t test or the Mann-Whitney U test was used to test the difference between groups for independent samples, and the paired samples t test or the Wilcoxon test was used for repeated measurement.
The associations between mortality and specific risk factors (age, gender, known coronary artery disease, diabetes mellitus [DM], hypertension, and donor type) were investigated with uni-variate analysis and then using forward-selection binary logistic regression analysis for multivariate analysis. Receiver–operating characteristic (ROC) curve analysis was carried out to calculate the area under the curve (AUC) to identify the best cutoff point for phase angle and albumin. The highest value for Youden index was accepted as the best cutoff value. Youden index was obtained from coordinates of the curve and calculated by “J¼ max [SN þ SP] 1.” The sensitivity and specificity of the cutoff values were also presented. The relative risk (RR) for the phase angle and albumin cutoff value was calculated for mortality.
Forward selection Cox multivariate regression was used to test the association of covariate variables (phase angle,
albumin, age, gender, DM, known coronary heart disease, and donor type) with survival.
All data analyses were performed with the IBM SPSS ver-sion 24 for Windows (IBM Corp, Armonk, New York) and was reported with 95% confidence intervals (CIs). Values of P < .05 were considered significant.
Findings
Demographic Characteristics, Clinical, and
Laboratory Data
Of the 158 kidney transplant recipients, 4 were lost to follow-up. The median follow-up time was 98 months (91-98 months). The initial demographic, clinical, and laboratory data for the 158 kidney transplant recipients are listed in Table 1. Study participants were caucasian, predominantly male (65.2%), mostly young or middle-aged, 37.5 (11.2), and had a living donor transplant (82.3%).
According to the body mass index (BMI), 31.6% of the recipients were overweight (BMI 25 kg/m2) and 15.8% were obese (BMI 30 kg/m2). The majority of the recipients had hypertension; however, systolic and diastolic blood pressure were generally normal. The prevalence of DM was low. Base-line GFR was >30 mL/min/1.73 m2 in all but 12 kidney
Table 1. Demographic, Clinical, and Laboratory Data and Bioimpedance Analysis of the Kidney Transplant Recipients From the Baseline Cross-Sectional Phase of the Study.
Mean (SD) Median (minimum-maximum)
Demographic data
Age (years) 37.5 (11.2) 36.0 (18.0-72.0)
Male gender (%) 65.2
Clinical data
Time from transplantation (months) 86.5 (56.5) 78.0 (12.0-282.0)
Living donor (%) 82.3
Height (cm) 164.8 (10.7) 165 (125.0-192.0)
Weight (kg) 69.0 (14.5) 70 (34.0-102.0)
Body mass index (kg/m2) 24.9 (4.5) 25 (15.0-40.0)
Systolic blood pressure (mm Hg) 122.5 (15.1) 120.0 (90.0-170.0)
Diastolic blood pressure (mm Hg) 76.5 (8.8) 80.0 (50.0-110.0)
Hypertension (%) 81
Diabetes mellitus (%) 8.9
Laboratory data
Serum creatinine (mg/dL) 1.43 (0.68) 1.28 (0.62-5.3)
Glomerular filtration rate (mL/min/1.73 m2) 63.0 (22.2) 62.5 (13.0-128.0)
High-density lipoprotein (mg/dL) 48.0 (13.1) 46.0 (24.0-90.0)
Triglycerides (mg/dL) 159.1 (87.7) 135 (37.0-644.0)
Albumin (mg/dL) 3.98 (0.46) 4 (1.74-5.0)
Fasting blood glucose (mg/dL) 89.3 (17.2) 87.5 (59.0-218.0)
Bioimpedance analysis
Resistance (ohms) 533.0 (86.4) 523.5 (298.0-794.0)
Reactance (ohms) 59.7 (12.2) 59.0 (320-91.0)
Phase angle () 6.4 (0.9) 6.4 (4.0-8.8)
Lean body mass (%) 75.9 (9.4) 75.4 (55.8-110.6)
Fat mass (%) 25.1 (9.0) 24.7 (2.9-65.0)
Extracellular fluid (%) 24.3 (3.2) 23.9 (17.5-37.4)
Intracellular fluid (%) 31.0 (5.0) 30.8 (18.5-46.5)
transplant recipients. Baseline BIA measurements calculated by BIA device are also shown in Table 1.
Follow-Up Data and Final Evaluation
As we could not contact 4 recipients, data were available for 154 recipients of the 158. Of these 154, one refused to answer questions regarding angina pectoris and claudication. Fifteen died during the follow-up period, 36 experienced CVE, and 4 developed cancer. Seven recipients experienced stroke. According to the Rose Questionnaire, 14 recipients had angina pectoris and 15 experienced a myocardial infarction. The Edin-burgh Claudication Questionnaire revealed 14 recipients with claudication. Twenty-six transplant recipients lost graft func-tionality; of those, 16 were currently on hemodialysis and 10 of them were retransplanted. The follow-up laboratory findings for kidney function in comparison between 2010 and 2018 are as follows: The mean creatinine value and MDRD stayed rel-atively stable changing from 1.43 (0.68) (median [minimum-maximum] as 1.28 [0.62-5.30], N¼ 158) mg/dL to 1.43 (0.64) (median [minimum-maximum] as 1.25 [0.47-4.07], N¼ 123) mg/dL (P < .001) and from 63.0 (22.2) (median [minimum-maximum] as 62.50 [13.0-128.0], N¼ 158) mL/min/1.73 m2
to 61.83 (25.6) (median [minimum-maximum] as 60.28 [14.03-185.24], N¼ 123) mL/min/1.73 m2
(P < .001), respectively. Data in 2018 were only available for the kidney transplant recipients preserving the graft functionality. The recipients who were retransplanted (N¼ 10) were also excluded there-fore, the following calculations were based on data of 123 kidney transplant recipients.
Determinants of Mortality
Univariate analysis revealed a significant difference between mortality and age, albumin, phase angle, intracellular fluid (%), and reactance parameters that can be obtained with BIA (P¼ .007, .001, .001, .018, and .011, respectively; Table 2). No significant difference was detected between mortality and gen-der, known coronary artery disease, DM, hypertension, donor
type, or other BIA parameters. These data are available in Supplementary Table 1.
In the forward-selection binary logistic regression, only phase angle and albumin persisted as independent risk factors for mortality (P¼ .020 and .010, respectively). These data are available in Supplementary Table 2. Model fit and Cohen k was found significant. The k coefficient, a measure of agree-ment, was low. Therefore, calculation of a cutoff value for phase angle and albumin would be more understandable. According to the ROC analysis, the cutoff value for phase angle regarding mortality was5.85, P ¼ .001 (AUC ¼ 76%, sensi-tivity¼ 67%, specificity ¼ 77%). Below that cutoff value, the RR for mortality was 5.33 (95% CI: 1.94-14.69, P ¼ .001), which means kidney transplant recipients with low phase angle (5.85) have 5.33-fold increased mortality risk compared to the others (phase angle > 5.85). The cutoff value for albumin was found to be3.72, P < .001 (AUC ¼ 79%, sensitivity ¼ 73%, specificity¼ 80%). Below that cutoff value, the RR for mortality was 8.25, which indicates an 8.25-fold increased risk for mortality in kidney transplant recipients with an albumin of 8.25 (95% CI: 2.79-24.39, P < .001). The ROC curves are shown in Figure 1. According to our results, we defined low phase angle as 5.85 and low albumin as
albumin3.72 mg/dL. However, in comparison of the ROC curves, we did not find any significant difference between phase angle and albumin regarding prediction of mortality (P¼ .576). Forward-selection Cox multivariate regression analysis was performed on 154 kidney transplant recipients for survival. Phase angle (5.85) and albumin (3.72) were significant; age, gender, DM, known coronary heart disease, and donor type were not significant covariates in survival. We found that a high phase angle (>5.85) and albumin (>3.72) were a protec-tive factor for survival. The hazard ratio (HR) in recipients with a low phase angle (5.85) was 3.36 which was associated with 3.36-fold increased risk of death (95% CI: 1.084-10.395, P¼ .036). The HR in recipients with low albumin (3.72) was 6.62 (95% CI: 1.984-22.083, P¼ .002), indicating that the risk of death in recipients with low albumin (3.72) was increased 6.62-fold.
Table 2. Univariate Analysis of BIA Parameters, Albumin, and Age According to Mortality. Alive, Mean (SD), N¼ 139 Median [Minimum-Maximum] Dead, Mean (SD), N¼ 15 Median [Minimum-Maximum] P Value Age 36.82 (10.81) 34.00 [1.00-68.00] 45.07 (12.52) 45.00 [18.00-72.00] .007a Albumin (mg/dL) 4.03 (0.41) 4.0 [2.25-5.00] 3.52 (0.61) 3.70 [1.74-4.40] .001a Phase angle () 6.49 (0.84) 6.50 [4.20-8.80] 5.67 (0.81) 5.80 [4.00-7.20] .001a Resistance (ohm) 531.91 (88.07) 519.00 [298.00-794.00] 535.07 (81.01) 523.00 [405.00-676.00] .930 Reactance (ohm) 60.12 (11.99) 60.00 [32.00-91.00] 52.73 (11.46) 51.00 [39.00-83.00] .011a
Lean body mass (%) 76.30 (9.30) 75.46 [55.92-110.58] 72.44 (10.15) 69.84 [55.79-96.32] .101
Fat mass (%) 24.95 (8.99) 24.60 [2.92-65.00] 27.05 (9.21) 27.09 [6.32-44.21] .258
Extracellular fluid (%) 24.37 (3.32) 23.71 [17.53-37.36] 24.48 (2.36) 24.54 [20.00-29.19] .476
Intracellular fluid (%) 31.28 (4.72) 31.11 [19.50-46.54] 27.84 (5.98) 27.21 [18.53-41.32] .018a
Abbreviations: BIA, bioelectrical impedance analysis; SD, standard deviation.
a
Mann-Whitney U Test.
Discussion
We found a statistically significant association between mor-tality and lower phase angle in kidney transplant recipients. In previous studies of dialysis patients, a significant association of nutritional status determined by BIA and survival has been shown.17-22 Phase angle was strongly associated with better survival in both peritoneal dialysis17 and hemodialysis patients.18 Moreover, the potential of phase angle predicting mortality has also been examined and shown previously in patients with cancer, intensive care unit patients, and patients with chronic heart failure.23-25 Saxena et al concluded in a study with kidney transplant recipients that higher phase angle was an indicator of good health regarding its capability of early prediction of deprived nutritional status.26 To the best of our knowledge, our study is the first study that shows an associa-tion between phase angle and mortality in kidney transplant recipients.
We calculated the threshold of phase angle for increased risk of mortality as 5.85. Below this cutoff value, phase angle could predict mortality during the 8-year follow-up with a sensitivity of 67% and specificity of 77%. In a larger study of dialysis patients (N ¼ 3009), phase angle <4 degrees was accepted as the threshold for increased risk of death in 1-year follow-up.27In another study, phase angle <6 has an RR of mortality per year of 4.1 compared to
those with a higher phase angle.26 Different cutoff values could be related to the patient population studied, duration of the follow-up period, and possibly to the type of BIA device.10Comparing the performance of phase angle in pre-dicting mortality with albumin, we did not detect any sta-tistically significant difference. Therefore, we can conclude phase angle is as good as albumin in prediction of mortality among kidney transplant recipients.
Bioelectrical impedance analysis is a relatively inexpensive, repeatable, and noninvasive method that makes the phase angle derived by BIA a good marker for long-term follow-up.28-29 Additionally, determining the phase angle does not require laboratory tests, body weight, or recalled parameters. It can be easily done with bedside measurements.24
Intracellular fluid and reactance were also associated with mortality. Intracellular fluid is a derivative of the raw measure-ment. Using raw BIA data rather than calculated values avoids bias related to variability inherited by estimated equations. Phase angle is also a raw BIA parameter expressed as the resistance to reactance ratio.11Therefore, it incorporates both those BIA parameters.
It is noteworthy that the fat content varies with gender, age, nutritional status, and even race.29However, in our study, we used phase angle as the primary variable; it has been accepted as a more stable BIA parameter.11
According to our statistical models, albumin and phase angle were independent predictors of mortality in kidney trans-plant recipients. The statistical model did not include age. We hypothesized that phase angle might be a surrogate marker for biological age, which is supposed to be a better marker for clinical outcomes than chronical age.30
There were 2 main limitations to our study. First, number of variables measured in our regression analysis was limited. Sec-ond, our study lacks serial follow-up of the BIA data. Serial measurements would add to the soundness of our results. Finally, we examined a selected population; the results may vary in other ethnic groups.
Conclusion
We showed for the first time that BIA analysis could be used as a surrogate marker for survival in kidney transplant recipients. The results of our study should be confirmed in different clin-ical and demographic settings, and our study cannot reveal pathogenic mechanism of this association. Therefore, it is not appropriate to provide specific management recommendations regarding low phase angle. However, we think that a close clinical follow-up and taking multiple measurements for each person might be considered for kidney transplant recipients with a low phase angle.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, author-ship, and/or publication of this article.
ORCID iD
Nurhan Seyahi https://orcid.org/0000-0001-7427-618X
Supplemental Material
Supplemental material for this article is available online. Figure 1. Receiver–operator curve of phase angle () and albumin
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