RESEARCH BRIEFS

Phase Angle Predicts Survival in Hemodialysis Patients Glenn M. Chertow, MD, MPH, *, J- Dunny 0. Jacobs, MD, MPH, f

/. Michael Lazams, MD, f Nancy L. Lew, SM, f and Edmund G. Lowvie, MDf

Objective: To determine the relation between phase angle by bioeiectrical impedance analysis (BIA) and survival in hemodialysis patients.

Design: Cohort analytic study. Setting: One hundred one free-standing outpatient dialysis units. Patients: Three thousand nine adult patients on thrice weekly hemodialysis. Patients with amputations above the

transmetatarsal site were excluded from participation. Main Outcome Measure: Vital status, with follow-up to at least 1 year. Results: Mean phase angle was 4.8 ? 1.8 degrees. Patients with narrow (low) phase angle experienced an

increased relative risk (RR) of death (<3 degrees; RR 4.3; 95% confidence interval [Cl], 2.9-6.2; and 3 to 4 degrees); RR 2.2; 95% Cl, 1.6-3.2; compared with the 26 degrees reference). There were no significant differences in risk among patients with phase angle 4 to 5 degrees (RR 1.2; 95% Cl, 0.8-l .8), 5 to 6 degrees (RR 1 .l; 95% Cl, 0.7-l .7), and 26 degrees, suggesting a nonlinear relation between phase angle and survival. The RRs for phase angle <4 degrees remained statistically significant after adjusting for age, gender, race, serum albumin and creatinine concentrations, and dialysis intensity (~3 degrees, RR 2.2; 95% Cl, 1.6-3.1, and 3 to 4 degrees, RR 1.3; 95% Cl, 1.0-l .7, compared with all patients 24 degrees).

Conclusions: In patients on hemodialysis, BIA-derived phase angle <4 degrees was associated with an increased RR of death, even after adjustment for case mix and several nutritional indicators. Further research is required to determine whether BIA can be used to monitor health status over time, or to gauge response to nutrition support or other clinical interventions in patients with end-stage renal disease. o 1997 by the National Kidney Foundation, Inc.

P ROTEIN ENERGY malnutrition afflicts a large fraction of hemodialysis (HD) pa-

tients,‘.” and it is an important determinant of mortality and morbidity.4-x Several methods of nutritional assessment have been applied in this population, including estimates of dietary intake, anthropometry, and biochemical tests, including

serum concentrations of creatinine, albumin, and

prealbumin. These biochemical indicators have

been shown repeatedly to predict survival in HD

patients, although their levels can be confounded by other disease processes (eg, liver disease, inflam-

mation, overhydration), and they do not capture the entire dimension of malnutrition. Body con-

position analysis has attracted some interest; how-

ever, most diagnostic methods are too costly and/or cumbersome to be applied in clinical

practice. Bioelectrical impedance analysis (BIA) has been

explored as a method of body composition analy- sis for more than a decade,” and it has recently

been applied to the dialysis population by several

groups of investigators. lo-l5 Briefly, bioelectrical

impedance (Z) is the vector sum of resistance (R) and reactance (Xc). Resistance is the opposition

204

ANTHROPOAfETRIC ASSESSME&-T OF ,WlTRITIOAAL STA’TW 177

body cell mass is the location of the body’s metabolic processes.’ At the tissue-system level, the body consists of adipose, muscle, and skeletal tissues. Adipose tissue is located in subcutaneous and visceral compartments, and its distribution on the body is under hormonal and genetic control. Skeletal muscle is the largest tissue component of the body accounting for about half the body weight in a healthy adult. Skeletal muscle consists of muscle tissue, nerves, tendons, and interstitial adipose tissue. The skeleton is the major reservoir of body minerals. Thus, body weight is the sum of the weights of adipose tissue, skeletal muscle, the skeleton and a residual of visceral organs nerves,

blood vessels and extracellular water. The intracel- lular water is included in the various tissues of the body.

There are direct and indirect methods of mea- suring body composition. Direct methods mea- sure specific chemical or anatomical constituents that are then used to calculate components of body composition. Direct methods tend to be accurate, but they can be invasive. Indirect meth- ods are frequently noninvasive but provide less accurate measures of body components that are used to predict body composition. Indirect esti- mates of body composition use measures of body weight and volume, bioelectrical impedance, body size, and subcutaneous adipose tissue m statistical models. These models are based on assumptions regarding the density of body tissues, the concen- trations of water and electrolytes in FFM and biological inter-relationships among normal indi- viduals. To be valid, indirect methods must be compared with results from direct methods. Indi- rect methods have larger errors for body composi- tion estimates than direct methods.

Anthropometry

Some body measurements commonly used in a nutrition assessment are listed in Table 1. Those measurements marked with an asterisk were col- lected in the Modification of Diet m Renal Disease (MDRD) Project and the current Hemo- dialysis (HEMO) study (Morbidity and Mortality in Hemodialysis Patients), two large multicenter studies of renal disease.sz” Stature and weight provide a general description of body size and mass. Body weight is a rough measure of total body energy stores. The triceps and subscapular skinfolds measure subcutaneous fat thickness on the limbs and trunk, and abdominal circumfer- ence is an index of internal adipose tissue.*” Calf circumference 1s an indirect measure of muscle mass.“,12 Elbow breadth is a useful measures of frame size, and knee height can be used to estimate stature.i3-‘j Body measurements can also be combined m indices that describe levels of body composition, nutritional status, or risk for disease.‘6-‘8 Stature and weight are used in the body mass index or BMI (weight/stature2 in kg/m’) to describe levels of body composition. Levels of BMI less than 19 and greater than 28 are associated with increased morbidity and mortal- ity.‘” Midarm circumference and triceps skinfold are combined to calculate midarm muscle area. Midarm muscle area and calf circumference are related to levels of protein stores or used as a marker for FFM. Anthropometric data are also used as covanates to help account for additional variance m statistical methods for estimating body composition.20

The use of standardized anthropometric tech- niques is important, especially if parameters of a nutrition assessment are compared with reference data or with data from related studies. There are

Table 1. Anthropometric Measurements Used in Assessing Nutrttional Status

Measurement Assessment Accuracv Rekabilitv Utrlitv

Stature* Weight*

Triceps skrnfold* Subscapular skinfold* Arm circumference*

Abdominal circumference Calf circumference* Knee height*

Elbow breadth*

Total body size Total body size Adipose tissue

Adipose tissue Fat-free mass and adipose tissue Adrpose tissue

Fat-free mass Lower leg length Body size

Very high

Very high Moderate Moderate

Hrgh Moderate Hrgh

High High

Very high

Very high Very high Moderate

Moderate Moderate Moderate

Hrgh Moderate

High High

Moderate Moderate Moderate

Moderate

High

Moderate

*Measured in MDRD or HEM0 studies.

178 WILLIAM CAMERON CHUMLEA

several texts that contain written techniques for the measurements listed in Table 1.21,” These

methods are the same or similar to those used by the National Center for Health Statistics to collect corresponding measurements in the Third Na- tional Health and Nutrition Examination Survey

(NHANES III). The anthropometric methods used in NHANES III were chosen to monitor the health and nutritional status of infants, children, adults, and the elderly. A video tape documenting the measurement techniques in NHANES III is

also available.23

Effects of Renal Disease on Anthropometric Data

Renal patients frequently present special prob-

lems for anthropometry.71 The assistance of two health technicians for the roles of examiner and recorder are generally required to accommodate the person’s health conditions. The examiner is

responsible for positioning the subject and taking each measurement. The recorder’s role is to assist the examiner in taking correct measurements by helping to position the subject and equipment to

ensure that accurate data are recorded. Measure- ments should be taken on the right side of the body because this side is used in all national reference data in the United States. However, if the patient has a vascular access, a cast, an

amputation or other limitations on the right side, it may be necessary to take measurements from the left side of the body. Also, placement of the vascular access in different parts of the body in hemodialysis patients will cause continuous shift-

mg of body locations for measurements of circum- ferences and skinfolds.

Some persons with renal problems may have difficulty standing or maintaining an erect posture and some are chair- or bed-fast. Recumbent anthropometric techniques are applicable to those renal patients who are unable to stand for measure-

ments. Recumbent measurements are reliable and accurate, and the values are not systematically different from those using corresponding standing techniques.2”

Because diabetes is one of the comorbid condi- tions with renal disease, some sufferers may experience amputations of the limbs due to vascular degeneration. Stature cannot be mea- sured accurately m these and other nonambula- tory individuals. The estimation of stature from

recumbent knee height with known errors is the

best method at present for providing this informa- tion for clinical and nutrition assessments.‘” For

those persons with bilateral amputations of the lower leg, there is presently no suitable method of estimating stature except for a self-report. Stature

prediction equations for persons with bilateral lower leg amputations will be available in the near future using measures of buttocks-knee length.

The measurement of weight in renal patients can require special equipment, such as bed or

wheelchair scales. Changes in weight parallel hydration status, energy, and protein balance. In adults, usual body weight varies less than +l.O

kg/d. A consistent loss in weight of more than 0.25 kg/d over time indicates negative energy or water balance, or a combination of the two.

Weight gain or loss, not associated with changes in body water, are associated with different rela- tive rates of change in the subcutaneous and

visceral adipose tissue compartments and from different anatomic sites. Measures of change in body weight should include anthropometric indi-

ces of body composition at regular but not frequent intervals. These measurements will pro-

vide a better understanding of the underlying parameters of a change in weight, such as alter- ations in the relative amounts and anatomical

distributions of adipose and muscle tissues.“s The effect of total body or regional alterations

in water content on anthropometric measure-

ments and body composition in patients with renal disease is not well defined. An abnormal hydration status alters the assumptions underlying

the methods and the density of the fat-free body and relationships with anthropometry. The level

of hydration affects skinfold and circumference measurements, and it is recommended that these be collected from the person after dialysis. Renal disease alters the water-based assumptions for body composition validated m normal indi- viduals.

In renal failure patients, edema may affect to a substantial degree estimates of FFM based on an assumed average hydration of 73%. Thus, m this water-retaining disease, the concept of FFM must be reassessed. Edema-free FFM may be a more useful nutrition parameter than FFM.a6 In other patients with chronic renal failure, total body potassium may not correlate closely with total body nitrogen, which is an indicator of total body protein. This indicates that in renal disease total

ANTHROPOMETRIC ASSESSMENT OF A’UTRITIOA’AL STATVS 179

body potassium may not be a suitable estimate of FFM.h

Limitations and Sources of Error

There are several limitations and sources of error for anthropometry.r’J7 The person being measured and the person taking the measure- ments are the major contributors to measurement error. If equipment is well-maintained and cali- brated, then it provides little to the overall errors. The limits of anthropometry are in their gross nature. Stature and weight used to calculate BMI provide only an index of body composition. A skinfold only measures a compressible amount of subcutaneous adipose tissue thickness at a specific location. The combination of the variances of the measurements affects the specific use of anthro- pometry. Regardless of the method selected, none are perfect, but frequently, the errors are ignored or forgotten. For an assessment of a renal patient, errors can have clinical relevance as the person is treated and observed over time.

Effects of Age, Gender, and Ethnicity on Anthropometric Data

The specific effects of renal disease on anthro- pometnc measures are further compounded by the normal effects of age, gender, and race of individual patients. Changes in body composition occur throughout the lifespan, and these are associated with corresponding changes in various physiologic functions that affect metabolism, nu- trient intake, physical activity, and risk of chronic diseases. Throughout childhood, there is an in- crease in the mineralization of the skeleton with growth and increases in the density of FFM.” In addition, the changes in the hormonal milieu alter the distribution and proportions of adipose, muscle, and skeletal tissues in children as they mature into adults. These changes are further affected by the variation among children in the onset and duration of maturation.

There is a decrease in the body cell mass with old age resulting from reductions m total body water, but there are conflicting reports regarding corresponding changes with age in extracellular water.‘s Changes in amounts of total body water and the proportion of mtercellular and extracellu- lar fluid volumes affect the relative hydration of FFM.a9

In addition. loss of bone mmeral with age requires changes in assumptions regarding the density of fat-free tissues. Bone mineral accounts for as much as 6% of FFM but decreases substan- tially after menopause. 30 Levels of FFM and bone mineral also decrease as physical activity decrease with hemodialysis. Changes in FFM and calf circumference may be due in part to decreased levels of physical activity. A significant negative correlation between age and calf circumference in elderly men, but not women, may be due to general loss of muscle in response to the reported greater reduction m physical activity among men than women. Losses of FFM with age may be due to reduced levels of physical activity reported in the elder1y.j’

Tinceps and subscapular skinfold thicknesses are significantly correlated with total and percent body fat m children and young adults.s2 In middle-aged adults and the elderly, body measure- ments, circumferences of the trunk, rather than skinfolds provide more information regarding stores of body fat. l2 With aging, adipose tissue thicknesses decrease on the arm and the leg as fat redistributes to the trunk, so that correlations of skinfold thicknesses with total and percent body fat are low. These changes are associated with poor limb and abdominal muscle structure or tone, as well as changes in fat patterning. Post- menopausal women are reported to have more upper-body fat than premenopausal women so that some changes may have endocrinologic sig- mficance. Changes in the elasticity, hydration, and compressibility of subcutaneous adipose and connective tissues in the elderly can also alter the relationship of anthropometry to body composi- tion and the interpretation of indices of adipose tissue drstnbution.

Ethnic differences m body composition are affected by differences m socioeconomic status, diet, use of health care and levels of genetic admixture. African-Americans have more dense bones and tend to have more bone mineral than non-Hispanics. 33 There are more African-Ameri- can women than non-Hispanic white women at the extremes of the distributions for body fatness. Data for body composition for large samples of African, Hispanic, or Asia-Americans are hm- ited.jGm3” However, reasonably extensive anthro- pometric data are available for African, Hispanic, and non-Hispanic white Americans from the NHANES survevs.

180 WILLIAM CAMERON CHUMLEA

Anthropometric Reference Data

The NHANES surveys are recognized for then

multiple methods of data collection includmg

interviews, physical examinations, physiological

testing, and biochemical assessments from a repre-

sentative sample of the United States popula-

tion.37 Mean values and distribution statistics for

stature, weight, and selected body circumfer- ences, breadths and skinfold thicknesses of chil-

dren and adults are available from the US Na-

tional Health Surveys. 38-41 Similar reference data

for the present US population will be available

from NHANES III in late 1997. However,

preliminary results from NHANES III, based on

percentiles for BMI, indicate that the prevalence

of obesity in the US adult population has in-

creased.4’,43 For African-American women, the

prevalence of obesity approaches 50% of the adult

population. The increased prevalence of obesity

in the US population raises serious questions

about the use of NHANES III data as a “health”

reference guide. Only limited anthropometric

reference data for persons with end stage renal

disease have been published.4i With the extensive

investigation of renal disease such as in the

HEM0 and MDRD Studies, current reference data for the body measurements of persons with

renal disease will become available in the future.

Summary

There are a variety of ways to assess nutritional

status. Some are sophisticated, others precise or

accurate, but the selection of a method depends

on what needs to be known and why. Persons with renal disease present a variety of problems to

renal dilutions for assessing nutntional status. The

effects of the disease alter many of the relation-

ships or assumptions between body measurements and body composition on which assessments are

based. These alterations combined with the de- creased functional status and increased comorbid-

ity associated with renal disease present a chal-

lenge to nutrition assessment methodology. In

meeting this challenge, the utility of anthropom- etry to renal dietitians as part of their nutrition

assessment screening armamentarium is signifi- cant, especially considering the relative cost and

the reference data available now and in the future.

Acknowledgment

The authors thank Dr. Shumei Guo (Wright State Umver-

stty School of Medrcme), Dr. Johanna Dwyer, Sandra Pow-

ers, Jerrllynn Burrowes, Roberta Henry (from the HEM0

Study), and David Cockram (Ross Products) for then helpful

comments and advtce.

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