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Ok Original ArticleVolume 53, Issue 3p571-577March 2017Open Archive Download Full Issue Download started Ok ASSOCIATION BETWEEN MULTI-FREQUENCY PHASE ANGLE AND SURVIVAL IN PATIENTS WITH ADVANCED CANCER David Hui, MD, MSc David Hui, MD, MSc Correspondence Address correspondence to: David Hui, MD, MSc, Department of Palliative Care, Rehabilitation and Integrative Medicine, University of Texas MD Anderson Cancer Center, Unit 1414, 1515 Holcombe Boulevard, Houston, TX 77030, USA. dhui@mdanderson.org Affiliations Department of Palliative Care and Rehabilitation Medicine, MD Anderson Cancer Center, Houston, USA Search for articles by this author a dhui@mdanderson.org ∙ Rony Dev, MD Rony Dev, MD Affiliations Department of Palliative Care and Rehabilitation Medicine, MD Anderson Cancer Center, Houston, USA Search for articles by this author a ∙ Lindsay Pimental, BSN Lindsay Pimental, BSN Affiliations Department of Palliative Care and Rehabilitation Medicine, MD Anderson Cancer Center, Houston, USA Search for articles by this author a ∙ … ∙ Minjeong Park, PhD Minjeong Park, PhD Affiliations Department of Biostatistics, MD Anderson Cancer Center, Houston, USA Search for articles by this author b ∙ Maria A. Cerana, MD Maria A. Cerana, MD Affiliations Department of Palliative Care and Rehabilitation Medicine, MD Anderson Cancer Center, Houston, USA Search for articles by this author a ∙ Diane Liu, MS Diane Liu, MS Affiliations Department of Biostatistics, MD Anderson Cancer Center, Houston, USA Search for articles by this author b ∙ Eduardo Bruera, MD Eduardo Bruera, MD Affiliations Department of Palliative Care and Rehabilitation Medicine, MD Anderson Cancer Center, Houston, USA Search for articles by this author a … Show more Show less Affiliations & NotesArticle Info aDepartment of Palliative Care and Rehabilitation Medicine, MD Anderson Cancer Center, Houston, USA bDepartment of Biostatistics, MD Anderson Cancer Center, Houston, USA Publication History: Accepted September 25, 2016; Published online December 30, 2016 DOI: 10.1016/j.jpainsymman.2016.09.016Also available on ScienceDirect Copyright: © 2016 American Academy of Hospice and Palliative Medicine. Published by Elsevier Inc. User License: Elsevier user license | Elsevier's open access license policy * Download PDFDownload PDF * Outline Outline * Abstract * Key Words * Introduction * Methods * Results * Discussion * Disclosures and Acknowledgements * References * Article metrics * Related Articles * Share SHARE Share on * Email * X * Facebook * LinkedIn * Sina Weibo * Add to Mendeley Add to my reading list * More More * Download PDFDownload PDF * Cite * Share SHARE Share on * Email * X * Facebook * LinkedIn * Sina Weibo * Add to Mendeley Add to my reading list * Set Alert * Get Rights * Reprints Download Full Issue Download started Ok Previous articleNext article Show Outline Hide Outline * Abstract * Key Words * Introduction * Methods * Results * Discussion * Disclosures and Acknowledgements * References * Article metrics * Related Articles ABSTRACT CONTEXT The ability to predict survival accurately has implications in clinical decision making. OBJECTIVES We determined the association of phase angle obtained from multi-frequency bioelectric impedance analysis with overall survival in patients with advanced cancer. METHODS We included consecutive patients with advanced cancer who had an outpatient palliative care consultation. Multi-frequency bioelectric impedance analysis assessed phase angle at three different frequencies (5/50/250 kHz) on each hemibody (right/left). Survival analysis was conducted using the Kaplan-Meier method, log-rank test, and multivariate Cox regression analysis. RESULTS Among 366 patients, the median overall survival was 250 days (95% confidence interval 191–303 days). The mean phase angle for 5, 50, and 250 kHz were 2.2°, 4.4°, and 4.2° on the right and 2.0°, 4.2° and 4.1° on the left, respectively. For all six phase angles, a lower value was significantly associated with a poorer overall survival (P < 0.001). After adjusting for cancer type, performance status, weight loss, and inflammatory markers, phase angle remained independently associated with overall survival (hazard ratio 0.85 per degree increase, 95% confidence interval 0.72–0.99; P = 0.048). CONCLUSION Phase angle represents a novel objective prognostic factor in outpatient palliative cancer care setting, regardless of frequency and body sides. KEY WORDS 1. Electric impedance 2. forecasting 3. neoplasms 4. palliative care 5. prognosis 6. survival INTRODUCTION In the advanced cancer setting, a patient's prognosis is an important determinant in clinical decision making. Recommendations regarding cancer treatments, palliative procedures, total parenteral nutrition, and hospice admissions are dependent on a patient's expected survival.1–3 1. Weeks, J.C. ∙ Cook, E.F. ∙ O'Day, S.J. ... Relationship between cancer patients' predictions of prognosis and their treatment preferences JAMA. 1998; 279:1709-1714 Crossref Scopus (1071) PubMed Google Scholar 2. Lamont, E.B. ∙ Christakis, N.A. Physician factors in the timing of cancer patient referral to hospice palliative care Cancer. 2002; 94:2733-2737 Crossref Scopus (95) PubMed Google Scholar 3. Miner, T.J. Palliative surgery for advanced cancer: lessons learned in patient selection and outcome assessment Am J Clin Oncol. 2005; 28:411-414 Crossref Scopus (45) PubMed Google Scholar Furthermore, an accurate understanding of prognosis allows patients and families to have a sense of control, prioritize their goals in life, and prepare for the end of life. Although many prognostic factors and prognostic models are available, they have not been used routinely in the clinical setting because of some key limitations, such as subjectivity, low accuracy, and difficulty in interpretation.4,5 4. Glare, P.A. ∙ Sinclair, C.T. Palliative medicine review: prognostication J Palliat Med. 2008; 11:84-103 Crossref Scopus (214) PubMed Google Scholar 5. Hui, D. Prognostication of survival in patients with advanced cancer: predicting the unpredictable? Cancer Control. 2015; 22:489-497 Crossref Scopus (146) PubMed Google Scholar Previous studies by our group and others have demonstrated that phase angle is a novel prognostic factor in patients with advanced cancer.6–8 6. Norman, K. ∙ Stobaus, N. ∙ Zocher, D. ... Cutoff percentiles of bioelectrical phase angle predict functionality, quality of life, and mortality in patients with cancer Am J Clin Nutr. 2010; 92:612-619 Crossref Scopus (273) PubMed Google Scholar 7. Santarpia, L. ∙ Marra, M. ∙ Montagnese, C. ... Prognostic significance of bioelectrical impedance phase angle in advanced cancer: preliminary observations Nutrition. 2009; 25:930-931 Full Text Full Text (PDF) Scopus (47) PubMed Google Scholar 8. Hui, D. ∙ Bansal, S. ∙ Morgado, M. ... Phase angle for prognostication of survival in patients with advanced cancer: preliminary findings Cancer. 2014; 120:2207-2214 Crossref Scopus (96) PubMed Google Scholar Phase angle is a function of cellular membrane integrity and hydration level.9 9. Norman, K. ∙ Stobaus, N. ∙ Pirlich, M. ... Bioelectrical phase angle and impedance vector analysis—clinical relevance and applicability of impedance parameters Clin Nutr. 2012; 31:854-861 Full Text Full Text (PDF) Scopus (670) PubMed Google Scholar It is typically assessed using single-frequency bioelectric impedance analysis (SF-BIA) at 50 Hz over the right side of the body. The development of multi-frequency bioelectric impedance analysis (MF-BIA) allows assessment of body composition at different frequencies that range from 1 to 1000 kHz typically. MF-BIAs have been found in several studies to have higher accuracy and greater precision compared with SF-BIAs in assessing body composition.10–14 10. Pietrobelli, A. ∙ Morini, P. ∙ Battistini, N. ... Appendicular skeletal muscle mass: prediction from multiple frequency segmental bioimpedance analysis Eur J Clin Nutr. 1998; 52:507-511 Crossref Scopus (83) PubMed Google Scholar 11. Gaba, A. ∙ Kapus, O. ∙ Cuberek, R. ... Comparison of multi- and single-frequency bioelectrical impedance analysis with dual-energy X-ray absorptiometry for assessment of body composition in post-menopausal women: effects of body mass index and accelerometer-determined physical activity J Hum Nutr Diet. 2015; 28:390-400 Crossref Scopus (62) PubMed Google Scholar 12. Martinoli, R. ∙ Mohamed, E.I. ∙ Maiolo, C. ... Total body water estimation using bioelectrical impedance: a meta-analysis of the data available in the literature Acta Diabetol. 2003; 40 Suppl 1:S203-S206 Crossref Scopus (68) PubMed Google Scholar 13. Raimann, J.G. ∙ Abbas, S.R. ∙ Liu, L. ... Agreement of single- and multi-frequency bioimpedance measurements in hemodialysis patients: an ancillary study of the Frequent Hemodialysis Network Daily Trial Nephron Clin Pract. 2014; 128:115-126 Crossref Scopus (15) PubMed Google Scholar 14. Teruel-Briones, J.L. ∙ Fernandez-Lucas, M. ∙ Ruiz-Roso, G. ... Analysis of concordance between the bioelectrical impedance vector analysis and the bioelectrical impedance spectroscopy in haemodialysis patients Nefrologia. 2012; 32:389-395 PubMed Google Scholar MF-BIA devices can also assess phase angle at different frequencies over the right and left hemibody. However, the utility of phase angle at different frequencies has not been examined in the palliative care population. A better understanding of the prognostic utility of phase angle at different frequencies may assist clinicians to estimate survival more accurately. In this study, we determined the association of six different phase angles (three frequencies and two sides of the body) with overall survival in patients with advanced cancer. METHODS STUDY SETTING AND CRITERIA This is a retrospective study of consecutive patients who had multi-frequency BIA completed between January 1, 2012, and March 31, 2014. Inclusion criteria included diagnosis of advanced cancer, defined as locally advanced, recurrent or metastatic disease for solid tumors or progressive/refractory/incurable disease for hematologic tumors, age 18 years or greater, and seen at the Supportive Care outpatient clinic. The Institutional Review Board at The University of Texas MD Anderson Cancer Center approved this study and waived the requirement for informed consent. DATA COLLECTION We collected baseline patient demographics on the day of multi-frequency BIA, including age, sex, race, cancer diagnosis (most active/serious cancer if multiple diagnoses), stage, and Eastern Cooperative Oncology Group performance status. We assessed phase angle using the InBody720 device (Inbody, Cerritos, CA). The test procedure was conducted according to the manufacturer's instructions. Ambulatory patients stepped on the multi-frequency BIA device with bare feet and held onto the hand rails bilaterally and remained on the device for two minutes. This analyzer uses an alternate current of 250 mA and assesses phase angle at 5, 50, and 250 kHz. The MF-BIA device measures segmental impedances at the right arm (RA), left arm (LA), right leg (RL), left leg (LL), and trunk (TR) for all three frequencies. The phase angle for the each half of body at each frequency is then calculated using the following formula: PAright=Atan[Xc(RA+TR+RL)/𝑅(RA+TR+RL)]PAleft=Atan[Xc(LA+TR+LL)/𝑅(LA+TR+LL)] where Xc is reactance and R is resistance. Symptom burden was assessed using the Edmonton Symptom Assessment Scale, a validated 10-item symptom battery examining average intensity of pain, fatigue, nausea, depression, anxiety, drowsiness, and shortness of breath, appetite, feeling of well–being, and sleep over the past 24 hours using numeric rating scales ranging from 0 (none) to 10 (worst).15,16 15. Bruera, E. ∙ Kuehn, N. ∙ Miller, M.J. ... The Edmonton Symptom Assessment System (ESAS): a simple method for the assessment of palliative care patients J Palliat Care. 1991; 7:6-9 Crossref PubMed Google Scholar 16. Nekolaichuk, C. ∙ Watanabe, S. ∙ Beaumont, C. The Edmonton Symptom Assessment System: a 15-year retrospective review of validation studies (1991–2006) Palliat Med. 2008; 22:111-122 Crossref Scopus (231) PubMed Google Scholar We also retrieved several objective laboratory-based prognostic variables that were collected within two weeks of phase angle, including leukocyte count, lymphocyte count, hemoglobin, serum albumin, calcium, and lactate dehydrogenase.8,17–22 8. Hui, D. ∙ Bansal, S. ∙ Morgado, M. ... Phase angle for prognostication of survival in patients with advanced cancer: preliminary findings Cancer. 2014; 120:2207-2214 Crossref Scopus (96) PubMed Google Scholar 17. Maltoni, M. ∙ Caraceni, A. ∙ Brunelli, C. ... Prognostic factors in advanced cancer patients: evidence-based clinical recommendations—a study by the Steering Committee of the European Association for Palliative Care J Clin Oncol. 2005; 23:6240-6248 Crossref Scopus (551) PubMed Google Scholar 18. Li, Q.Q. ∙ Lu, Z.H. ∙ Yang, L. ... Neutrophil count and the inflammation-based glasgow prognostic score predict survival in patients with advanced gastric cancer receiving first-line chemotherapy Asian Pac J Cancer Prev. 2014; 15:945-950 Crossref Scopus (84) PubMed Google Scholar 19. Petrelli, F. ∙ Cabiddu, M. ∙ Coinu, A. ... Prognostic role of lactate dehydrogenase in solid tumors: a systematic review and meta-analysis of 76 studies Acta Oncol. 2015; 54:961-970 Crossref Scopus (220) PubMed Google Scholar 20. Templeton, A.J. ∙ McNamara, M.G. ∙ Seruga, B. ... Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis J Natl Cancer Inst. 2014; 106:dju124 Crossref Scopus (2216) PubMed Google Scholar 21. Zhang, J. ∙ Yao, Y.H. ∙ Li, B.G. ... Prognostic value of pretreatment serum lactate dehydrogenase level in patients with solid tumors: a systematic review and meta-analysis Scientific Rep. 2015; 5:9800 Crossref Scopus (93) PubMed Google Scholar 22. Donovan, P.J. ∙ Achong, N. ∙ Griffin, K. ... PTHrP-mediated hypercalcemia: causes and survival in 138 patients J Clin Endocrinol Metab. 2015; 100:2024-2029 Crossref Scopus (77) PubMed Google Scholar Survival from time of multi-frequency BIA assessment was collected from institutional databases and electronic health records. STATISTICAL ANALYSES We summarized the baseline demographics using descriptive statistics, including mean, SD, median, interquartile range, frequency, and percentage. We examined the association between pairwise phase angle by frequency and body side using the Spearman rank correlation test. We estimated overall survival using the Kaplan-Meier method and compared among degrees of phase angle using the log-rank test. We used the Contal and O'Quigley method to identify the optimal cutoff of a phase angle for overall survival.23 23. Contal, C. ∙ O'Quigley, J. An application of changepoint methods in studying the effect of age on survival in breast cancer Comput Stat Data Anal. 1999; 30:253-270 Crossref Scopus (489) Google Scholar We then applied this survival analysis to other laboratory variables based on predefined, established cutoffs from the literature, including leukocytosis (serum leukocyte >11,000/mm3), lymphopenia (lymphocyte <1%), anemia (hemoglobin <8.0 g/dL), neutrophil-lymphocyte ratio >3, hypoalbuminemia (serum albumin <4.0 g/dL), hypercalcemia (corrected calcium >10.2 mg/dL), and elevated lactate dehydrogenase (>618 IU/L).18,22 18. Li, Q.Q. ∙ Lu, Z.H. ∙ Yang, L. ... Neutrophil count and the inflammation-based glasgow prognostic score predict survival in patients with advanced gastric cancer receiving first-line chemotherapy Asian Pac J Cancer Prev. 2014; 15:945-950 Crossref Scopus (84) PubMed Google Scholar 22. Donovan, P.J. ∙ Achong, N. ∙ Griffin, K. ... PTHrP-mediated hypercalcemia: causes and survival in 138 patients J Clin Endocrinol Metab. 2015; 100:2024-2029 Crossref Scopus (77) PubMed Google Scholar The Cox proportional hazard model was used to assess the effect of phase angle on overall survival, adjusting for patient characteristics and the objective laboratory-based prognostic factors. Stepwise selection was used to build the final multivariate model that included all covariates with P-value <0.05 in univariate analysis. All computations were carried out in SAS 9.3 (SAS Institute, Cary, NC), Splus 8.2 (TIBCO software Inc, Palo Alto, CA), and R 3.1.3 (University of Twente, Enschede, The Netherlands). A P-value <0.05 is considered to be statistically significant. RESULTS PATIENT CHARACTERISTICS Table 1 lists the baseline characteristics of 366 patients at time of multi-frequency BIA assessment. The median age was 58 (range 21–90), 168 (46%) were female, and 242 (66%) were white. The most common cancer diagnoses were gastrointestinal (n = 111, 30%), breast cancer (n = 50, 14%), and head and neck cancer (n = 48, 13%). The median overall survival of this cohort was 250 days (95% confidence interval 191–303 days). Among the patients alive, the median followup was 924 days. Characteristicsn (%)aAge, average (range)58 (21–90)Female sex168 (46)RaceWhite242 (66)Black59 (16)Hispanic39 (11)Other26 (7)Cancer typeBreast50 (14)Gastrointestinal111 (30)Genitourinary20 (6)Gynecological34 (9)Head and neck48 (13)Hematologic8 (2)Respiratory40 (11)Other55 (15)Edmonton Symptom Assessment Scale, mean (SD)Pain4.2 (3.0)Fatigue5.2 (2.9)Nausea2.0 (2.7)Depression2.7 (2.9)Anxiety3.1 (3.1)Drowsiness3.5 (3.1)Dyspnea3.1 (3.2)Appetite4.7 (3.1)Well being4.5 (2.9)Sleep4.7 (2.9)ECOG Performance status0–181 (22.6)2147 (41.1)3130 (36.3)40Percentage weight loss over past 6 months, mean (SD)7.8 (14.6)Serum albumin in g/dL, mean (SD)3.8 (.7)Hypercalcemia (corrected calcium >10.2 mg/dL)11 (4.1)Lactate dehydrogenase in unit, mean (SD)778.5 (1226.2)Leukocytosis (serum leukocyte >11,000/mm3)40 (12.0)Lymphopenia (lymphocyte <1%)140 (42.2)Anemia (hemoglobin <8.0 g/dL)13 (3.9)Neutrophil-lymphocyte ratio, mean (SD)5.9 (7.0) Table 1 Baseline Characteristics (N = 366) ECOG = Eastern Cooperative Oncology Group. a Unless otherwise specified. * Open table in a new tab PHASE ANGLE VALUES Table 2 illustrates the average phase angle values by frequency and body side. The values for 50 and 250 kHz were comparable, although the values for 5 kHz were significantly lower. Frequency/Hemibody≤2°, n (%)>2–3°, n (%)>3–4°, n (%)>4–5°, n (%)>5–6°, n (%)>6°, n (%)Mean (SD)5 kHz right161 (44)167 (46)27 (7)7 (2)2 (0.6)2 (0.6)2.2 (0.8)50 kHz right4 (1)24 (7)105 (29)133 (36)83 (23)17 (5)4.4 (1.0)250 kHz right1 (0.3)7 (2)122 (33)211 (58)23 (6)2 (0.6)4.2 (0.6)5 kHz left184 (50)163 (45)17 (5)2 (0.6)0 (0)0 (0)2.0 (0.6)50 kHz left5 (1)25 (7)125 (34)132 (36)68 (19)11 (3)4.2 (1.0)250 kHz left0 (0)9 (3)137 (37)201 (55)18 (5)1 (0.3)4.1 (0.6) Table 2 Distribution of Phase Angle * Open table in a new tab Phase angle values between the right and left side of the body were also highly similar (Table 2). The Spearman correlation coefficient (ρ) between left and right side were 0.85, 0.91, and 0.87 for 5, 50, and 250 kHz, respectively (Table 3). The lowest level of correlation was between the left 250 kHz measurement and right-sided 5 kHz measurement (ρ = 0.56, P < 0.001). We found that phase angle was significantly associated with age, sex, and body mass index at all frequencies and both sides, with the only exception at 250 kHz for sex (data not shown). Frequency/Hemibody5 kHz Right50 kHz Right250 kHz Right5 kHz Left50 kHz Left250 kHz Left5 kHz right— 50 kHz right0.79— 250 kHz right0.630.85— 5 kHz left0.850.800.63— 50 kHz left0.720.910.760.82— 250 kHz left0.560.780.870.630.84— Table 3 Correlation Among Phase Angle at Different Frequenciesa a All P-values <0.0001 from Spearman Rank Correlation test. * Open table in a new tab SURVIVAL ANALYSIS Univariate analysis was conducted with cutoff based on log-rank test when phase angle was analyzed by degree (Table 4). A lower phase angle was associated with worse survival in all six measures (Fig. 1). In multivariate analysis adjusting for patient characteristics and many known objective laboratory variables, phase angle remained significantly associated with overall survival (hazard ratio 0.85 per degree increase in phase angle, 95% CI 0.72–0.99; P = 0.048; Table 4). Figure viewer Fig. 1 Kaplan-Meier survival curves by phase angle. Overall survival was calculated from time of study assessment to last follow-up date or death. Cutoffs based on the Contal and O'Quigley method. Univariate AnalysisMultivariate AnalysesaHazard Ratio (95% CI)P-ValueHazard Ratio (95% CI)P-ValueAge (per year increase)1.004 (0.99–1.01)0.45 Male sex (vs. female)0.97 (0.76–1.24)0.82 RaceAsian vs. white1.16 (0.69–1.93)0.21 Black vs. white1.19 (0.86–1.65) Hispanic vs. white1.31 (0.88–1.96) Other vs. white2.71 (1.001–7.36) Cancer typeBreast vs. respiratory0.70 (0.43–1.15)<0.0001 Gastrointestinal vs. respiratory1.36 (0.90–2.07) Genitourinary vs. respiratory0.73 (0.39–1.38) Gynecological vs. respiratory1.64 (0.98–2.74) Head and neck vs. respiratory0.39 (0.23–0.68) Hematologic vs. respiratory1.35 (0.56–3.26) Other vs. respiratory0.69 (0.42–1.12) ECOG performance status1.77 (1.49–2.11)<.00011.53 (1.25–1.89)<0.0001Percentage weight loss over past 6 months0.98 (0.97–0.99)0.02 Hypoalbuminemia (serum albumin <4.0 g/dL)2.42 (1.82–3.21)<0.00011.71 (1.24–2.36)0.001Hypercalcemia (corrected calcium >10.2 mg/dL)1.82 (0.85–3.87)0.12 Elevated lactate dehydrogenase (>618 unit)2.43 (1.81–3.26)<0.00012.18 (1.59–2.98)<0.0001Leukocytosis (serum leukocyte >11,000/mm3)1.55 (1.06–2.26)0.02 Lymphopenia (lymphocyte % <1%)1.63 (1.26–2.10)0.0002 Anemia (hemoglobin <8.0 g/dL)1.42 (0.77–2.60)0.26 Neutrophil-lymphocyte ratio >32.02 (1.53–2.66)<0.00011.65 (1.20–2.28)0.002Phase angle (per degree increase)5 kHz right0.76 (0.64–0.90)0.002 50 kHz right0.72 (0.64–0.82)<0.00010.85 (0.72–0.99)0.048250 kHz right0.65 (0.54–0.79)<0.0001 5 kHz left0.60 (0.49–0.74)<0.0001 50 kHz left0.71 (0.62–0.80)<0.0001 250 kHz left0.69 (0.56–0.84)<0.0001 Table 4 Univariate and Multivariate Cox Regression Analyses ECOG = Eastern Cooperative Oncology Group. a Covariates with P-value <0.05 were included in the multivariate Cox Regression Model and included cancer type, percentage weight loss, ECOG performance status, hypoalbuminemia, elevated lactate dehydrogenase, leukocytosis, lymphopenia, neutrophil-lymphocyte ratio, and phase angle 50 kHz right. We only entered one of six phase angles in the model because they were all highly correlated with each other. We selected 50 kHz right because it is most often used in single-frequency assessments. Stepwise selection was used to build the final multivariate model. * Open table in a new tab DISCUSSION To our knowledge, this is the first study to examine phase angle at different frequencies measured using MF-BIA in the palliative care setting. We found that phase angle was strongly associated with survival in patients with advanced cancer. Survival prediction was highly similar among the different frequencies and between the two sides of the body. On further validation, this objective, noninvasive and relatively inexpensive prognostic tool may be useful to support clinical decision making. Multiple studies have reported that low phase angle is associated with poorer survival in cancer and noncancer patients.8,24–27 8. Hui, D. ∙ Bansal, S. ∙ Morgado, M. ... Phase angle for prognostication of survival in patients with advanced cancer: preliminary findings Cancer. 2014; 120:2207-2214 Crossref Scopus (96) PubMed Google Scholar 24. Schwenk, A. ∙ Beisenherz, A. ∙ Romer, K. ... Phase angle from bioelectrical impedance analysis remains an independent predictive marker in HIV-infected patients in the era of highly active antiretroviral treatment Am J Clin Nutr. 2000; 72:496-501 Crossref Scopus (236) PubMed Google Scholar 25. Mushnick, R. ∙ Fein, P.A. ∙ Mittman, N. ... Relationship of bioelectrical impedance parameters to nutrition and survival in peritoneal dialysis patients Kidney Int. 2003; 87:S53-S56 Full Text Full Text (PDF) Scopus (132) Google Scholar 26. Desport, J.C. ∙ Marin, B. ∙ Funalot, B. ... Phase angle is a prognostic factor for survival in amyotrophic lateral sclerosis Amyotroph Lateral Scler. 2008; 9:273-278 Crossref Scopus (52) PubMed Google Scholar 27. Abad, S. ∙ Sotomayor, G. ∙ Vega, A. ... The phase angle of the electrical impedance is a predictor of long-term survival in dialysis patients Nefrologia. 2011; 31:670-676 PubMed Google Scholar However, only a handful of studies have specifically focused on the advanced cancer population, in which the survival was relatively homogeneous.6,28,29 6. Norman, K. ∙ Stobaus, N. ∙ Zocher, D. ... Cutoff percentiles of bioelectrical phase angle predict functionality, quality of life, and mortality in patients with cancer Am J Clin Nutr. 2010; 92:612-619 Crossref Scopus (273) PubMed Google Scholar 28. Davis, M.P. ∙ Yavuzsen, T. ∙ Khoshknabi, D. ... Bioelectrical impedance phase angle changes during hydration and prognosis in advanced cancer Am J Hosp Palliat Care. 2009; 26:180-187 Crossref Scopus (36) PubMed Google Scholar 29. Lee, S.Y. ∙ Lee, Y.J. ∙ Yang, J.H. ... The association between phase angle of bioelectrical impedance analysis and survival time in advanced cancer patients: preliminary study Korean J Fam Med. 2014; 35:251-256 Crossref Scopus (39) PubMed Google Scholar In a recent study by our group, we enrolled 222 hospitalized patients with advanced cancer who were seen by palliative care team for consultation. The median survival was 106 days, and lower phase angle (assessed with SF-BIA) was associated with worse survival independent of other known prognostic variables, such as the Palliative Prognostic Score, Palliative Prognostic Index, lean body mass, and hypoalbumenia.8 8. Hui, D. ∙ Bansal, S. ∙ Morgado, M. ... Phase angle for prognostication of survival in patients with advanced cancer: preliminary findings Cancer. 2014; 120:2207-2214 Crossref Scopus (96) PubMed Google Scholar Because survival can differ substantially between patients seen by inpatient and outpatient palliative care, our present study contributes to the literature by documenting phase angle values in ambulatory palliative care setting. With median survival of 250 days, the mean phase angle was 4.4 (SD 1.0). In contrast to single-frequency BIA which is most often conducted at 50 kHz, MF-BIAs assess impedance at different frequencies ranging between 1 and 1000 kHz. Lower frequency currents (<50 kHz) generally flows through the extracellular compartment, whereas higher frequency currents (>200 kHz) can penetrate cell membranes and pass through lean tissues.30 30. Utter, A.C. ∙ Nieman, D.C. ∙ Mulford, G.J. ... Evaluation of leg-to-leg BIA in assessing body composition of high-school wrestlers Med Sci Sports Exerc. 2005; 37:1395-1400 Crossref Scopus (23) PubMed Google Scholar This differential tissue penetration at various frequencies allows fat free mass, total body water, intracellular water, and extracellular water to be delineated and measured accurately.31,32 31. Kyle, U.G. ∙ Bosaeus, I. ∙ De Lorenzo, A.D. ... Bioelectrical impedance analysis—part I: review of principles and methods Clin Nutr. 2004; 23:1226-1243 Full Text Full Text (PDF) Scopus (2148) PubMed Google Scholar 32. Kyle, U.G. ∙ Bosaeus, I. ∙ De Lorenzo, A.D. ... Bioelectrical impedance analysis—part II: utilization in clinical practice Clin Nutr. 2004; 23:1430-1453 Full Text Full Text (PDF) Scopus (1610) PubMed Google Scholar Several studies reported that MF-BIA was either comparable or more accurate than SF-BIA for assessment of body composition in healthy subjects10,11 10. Pietrobelli, A. ∙ Morini, P. ∙ Battistini, N. ... Appendicular skeletal muscle mass: prediction from multiple frequency segmental bioimpedance analysis Eur J Clin Nutr. 1998; 52:507-511 Crossref Scopus (83) PubMed Google Scholar 11. Gaba, A. ∙ Kapus, O. ∙ Cuberek, R. ... Comparison of multi- and single-frequency bioelectrical impedance analysis with dual-energy X-ray absorptiometry for assessment of body composition in post-menopausal women: effects of body mass index and accelerometer-determined physical activity J Hum Nutr Diet. 2015; 28:390-400 Crossref Scopus (62) PubMed Google Scholar and patients on hemodialysis.13,14 13. Raimann, J.G. ∙ Abbas, S.R. ∙ Liu, L. ... Agreement of single- and multi-frequency bioimpedance measurements in hemodialysis patients: an ancillary study of the Frequent Hemodialysis Network Daily Trial Nephron Clin Pract. 2014; 128:115-126 Crossref Scopus (15) PubMed Google Scholar 14. Teruel-Briones, J.L. ∙ Fernandez-Lucas, M. ∙ Ruiz-Roso, G. ... Analysis of concordance between the bioelectrical impedance vector analysis and the bioelectrical impedance spectroscopy in haemodialysis patients Nefrologia. 2012; 32:389-395 PubMed Google Scholar A meta-analysis of 16 studies also reported the MF-BIA was more accurate than SF-BIA in estimating total body water in patients with CKD.12 12. Martinoli, R. ∙ Mohamed, E.I. ∙ Maiolo, C. ... Total body water estimation using bioelectrical impedance: a meta-analysis of the data available in the literature Acta Diabetol. 2003; 40 Suppl 1:S203-S206 Crossref Scopus (68) PubMed Google Scholar More studies are needed to assess the utility of MF-BIA compared with SF-BIA in assessing body composition in the oncology setting. To date, only a handful of studies have reported the use of MF-BIA in survival prediction. O'Lone included 529 patients on peritoneal dialysis and reported that the overhydration to extracellular water ratio was an independent predictor of mortality when the BMI and lean tissue index were included in multivariate model.33 33. O'Lone, E.L. ∙ Visser, A. ∙ Finney, H. ... Clinical significance of multi-frequency bioimpedance spectroscopy in peritoneal dialysis patients: independent predictor of patient survival Nephrol Dial Transpl. 2014; 29:1430-1437 Crossref Scopus (99) PubMed Google Scholar Caravaca et al. reported that phase angle at 50 kHz was associated with mortality (hazard ratio = 0.49; P = 0.026) in 175 patients with chronic kidney disease.34 34. Caravaca, F. ∙ Martinez del Viejo, C. ∙ Villa, J. ... Hydration status assessment by multi-frequency bioimpedance in patients with advanced chronic kidney disease Nefrologia. 2011; 31:537-544 PubMed Google Scholar Few groups have studied phase angle at other frequencies. Malecka-Massalska et al. examined phase angle at 5, 50, 100, and 200 kHz in 31 patients with head and neck cancer and reported that phase angle was also significantly lower than normal control at all frequencies.35 35. Malecka-Massalska, T. ∙ Smolen, A. ∙ Morshed, K. Altered tissue electrical properties in squamous cell carcinoma in head and neck tumors: preliminary observations Head Neck. 2013; 35:1101-1105 Crossref Scopus (14) PubMed Google Scholar Moreover, phase angle significantly decreased at followup after surgery at all frequencies except 200 kHz.36 36. Malecka-Massalska, T. ∙ Smolen, A. ∙ Morshed, K. Tissue electrical properties in head and neck tumors before and after surgery: preliminary observations Ind J Cancer. 2014; 51:209-213 Crossref Scopus (6) PubMed Google Scholar Sarode et al. examined phase angle at 20 Hz, 50 kHz, 1.3 MHz, 2.5 MHz, 3.7 MHz, and 5 MHz in 100 individuals and reported that phase angle decreased with increasing frequency.37 37. Sarode, G.S. ∙ Sarode, S.C. ∙ Kulkarni, M. ... Bioimpedance assessment of oral squamous cell carcinoma with clinicopathological correlation J Contemp Dent Pract. 2015; 16:715-722 Crossref Scopus (4) PubMed Google Scholar Given the differential tissue penetration, phase angle assessed at 5, 50, and 250 kHz could potentially provide different prognostic information. We found that the phase angle values at 50 and 250 kHz were comparable with each other, whereas the phase angle values at 5 kHz were significantly lower. There was also a high level of correlation between the left and right side of the body, which was not surprising. Importantly, a lower phase angle value was consistently associated with shorter survival and the phase angle at the three frequencies provided similar level of discrimination. The implications of our findings are as follows: (1) phase angle at 50 kHz alone is a reasonable measure because it is most frequently used and reference data are available,38 38. Barbosa-Silva, M.C. ∙ Barros, A.J. ∙ Wang, J. ... Bioelectrical impedance analysis: population reference values for phase angle by age and sex Am J Clin Nutr. 2005; 82:49-52 Crossref PubMed Google Scholar (2) phase angle at other frequencies may also be informative and strongly correlate with 50 kHz, and (3) further research is needed to examine if phase angle at other frequencies outside our range (i.e., <5 or >250 kHz) remain accurate for prognostication of survival. We recently reported that objective prognostic factors have higher accuracy than clinician prediction of survival alone, supporting the use of objective measures for prognostication.39 39. Hui, D. ∙ Park, M. ∙ Liu, D. ... Clinician prediction of survival versus the Palliative Prognostic Score: which approach is more accurate? Eur J Cancer. 2016; 64:89-95 Full Text Full Text (PDF) Scopus (61) PubMed Google Scholar Here, we found that phase angle was a predictor of survival independent of many established objective laboratory markers, such as hypoalbuminemia, leukocytosis, neutrophil-to-leukocyte ratio, and elevated lactate dehydrogenase. This may be because phase angle assesses a different physiological aspect than these other variables. Further studies are needed to compare the accuracy of these measures and to derive a prognostic score based solely on objective variables that can have high accuracy. This study has several limitations. First, the retrospective nature of data gathering means that we were not able to include several key prognostic variables, such as the Palliative Prognostic Score and C-reactive protein. Second, patients need to be able to stand on the scale for a few minutes to use the Inbody 720 device. Thus, a few individuals seen at the outpatient clinic were excluded because of muscle weakness. Thus, the Inbody 720 device may not be feasible in the inpatient setting, although other MF-BIAs are available that can be conducted with patient in a supine position. In summary, phase angle represents a novel objective prognostic factor in outpatient palliative cancer care setting, regardless of frequency and body sides. Future studies should examine how phase angle values can be used to inform both patients with advanced cancer and clinicians in decision making on the many complex issues in the last months of life, such as palliative procedures, chemotherapy and nutrition. DISCLOSURES AND ACKNOWLEDGEMENTS This work was supported by the National Institutes of Health Cancer Center Support Grant (CA016672 to Drs Park and Liu). Dr. Hiu is supported in part by a National Institutes of Health grant (R21CA186000–01A1), an American Cancer Society Mentored Research Scholar Grant in Applied and Clinical Research (MRSG-14–1418-01-CCE), and an institutional startup grant (#18075582). The study device was provided by Inbody USA on loan. The company had no role in study design, data collection, analysis, interpretation, or writing of the report. The authors declare no conflicts of interest. REFERENCES 1. Weeks, J.C. ∙ Cook, E.F. ∙ O'Day, S.J. ... Relationship between cancer patients' predictions of prognosis and their treatment preferences JAMA. 1998; 279:1709-1714 Crossref Scopus (1071) PubMed Google Scholar 2. Lamont, E.B. ∙ Christakis, N.A. Physician factors in the timing of cancer patient referral to hospice palliative care Cancer. 2002; 94:2733-2737 Crossref Scopus (95) PubMed Google Scholar 3. Miner, T.J. 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Phase angle is a prognostic factor for survival in amyotrophic lateral sclerosis Amyotroph Lateral Scler. 2008; 9:273-278 Crossref Scopus (52) PubMed Google Scholar 27. Abad, S. ∙ Sotomayor, G. ∙ Vega, A. ... The phase angle of the electrical impedance is a predictor of long-term survival in dialysis patients Nefrologia. 2011; 31:670-676 PubMed Google Scholar 28. Davis, M.P. ∙ Yavuzsen, T. ∙ Khoshknabi, D. ... Bioelectrical impedance phase angle changes during hydration and prognosis in advanced cancer Am J Hosp Palliat Care. 2009; 26:180-187 Crossref Scopus (36) PubMed Google Scholar 29. Lee, S.Y. ∙ Lee, Y.J. ∙ Yang, J.H. ... The association between phase angle of bioelectrical impedance analysis and survival time in advanced cancer patients: preliminary study Korean J Fam Med. 2014; 35:251-256 Crossref Scopus (39) PubMed Google Scholar 30. Utter, A.C. ∙ Nieman, D.C. ∙ Mulford, G.J. ... Evaluation of leg-to-leg BIA in assessing body composition of high-school wrestlers Med Sci Sports Exerc. 2005; 37:1395-1400 Crossref Scopus (23) PubMed Google Scholar 31. Kyle, U.G. ∙ Bosaeus, I. ∙ De Lorenzo, A.D. ... Bioelectrical impedance analysis—part I: review of principles and methods Clin Nutr. 2004; 23:1226-1243 Full Text Full Text (PDF) Scopus (2148) PubMed Google Scholar 32. Kyle, U.G. ∙ Bosaeus, I. ∙ De Lorenzo, A.D. ... Bioelectrical impedance analysis—part II: utilization in clinical practice Clin Nutr. 2004; 23:1430-1453 Full Text Full Text (PDF) Scopus (1610) PubMed Google Scholar 33. O'Lone, E.L. ∙ Visser, A. ∙ Finney, H. ... Clinical significance of multi-frequency bioimpedance spectroscopy in peritoneal dialysis patients: independent predictor of patient survival Nephrol Dial Transpl. 2014; 29:1430-1437 Crossref Scopus (99) PubMed Google Scholar 34. Caravaca, F. ∙ Martinez del Viejo, C. ∙ Villa, J. ... Hydration status assessment by multi-frequency bioimpedance in patients with advanced chronic kidney disease Nefrologia. 2011; 31:537-544 PubMed Google Scholar 35. Malecka-Massalska, T. ∙ Smolen, A. ∙ Morshed, K. Altered tissue electrical properties in squamous cell carcinoma in head and neck tumors: preliminary observations Head Neck. 2013; 35:1101-1105 Crossref Scopus (14) PubMed Google Scholar 36. Malecka-Massalska, T. ∙ Smolen, A. ∙ Morshed, K. Tissue electrical properties in head and neck tumors before and after surgery: preliminary observations Ind J Cancer. 2014; 51:209-213 Crossref Scopus (6) PubMed Google Scholar 37. Sarode, G.S. ∙ Sarode, S.C. ∙ Kulkarni, M. ... Bioimpedance assessment of oral squamous cell carcinoma with clinicopathological correlation J Contemp Dent Pract. 2015; 16:715-722 Crossref Scopus (4) PubMed Google Scholar 38. Barbosa-Silva, M.C. ∙ Barros, A.J. ∙ Wang, J. ... Bioelectrical impedance analysis: population reference values for phase angle by age and sex Am J Clin Nutr. 2005; 82:49-52 Crossref PubMed Google Scholar 39. Hui, D. ∙ Park, M. ∙ Liu, D. ... Clinician prediction of survival versus the Palliative Prognostic Score: which approach is more accurate? Eur J Cancer. 2016; 64:89-95 Full Text Full Text (PDF) Scopus (61) PubMed Google Scholar FIGURES (1)FIGURE VIEWER ARTICLE METRICS Metric data currently unavailable RELATED ARTICLES We haven't found any related articles. 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