Assessment of Urea Appearance Rates and Net Nitrogen Deficits in Patients With Acute Renal Failure Receiving Continuous Venovenous Hemofiltration

Original Research

Assessment of Urea Appearance Rates and Net Nitrogen Deficits in Patients With Acute Renal Failure Receiving Continuous Venovenous Hemofiltration Mary H. Murphy, MS, RD, CNSD ,* Karla J. Alaka, RD,t Michael E. Miller, PhD,:j: and William L. Macias , MD, PhD§ • Objective: To investigate the impact of the nutritional reg imen on the urea appearance rate (UAR) and net nitrogen deficit (NND) in patients with acute renal failure (ARF) receiving continuous venovenous hemofiltration (CWH) . Comparison of estimated energy expenditure using a modification ofthe Harris-Benedict equation versus measured energy expenditure was performed. • Design : Noninterventional study with prospective data collection . • Setting: Tertiary care hospital. • Patients: Forty consecutive patients age 52 ± 20 years (mean ± SD) with ARF who required CWH between June 1991 and June 1992. • Interventions: Noninterventional study. • Main outcome measures: UAR and NND were calculated for each study day. Total calories , nonprotein calories , and grams of protein per day, and estimated energy needs were quantified for all patients. Energy expenditure was measured for 10 patients. • Results: Patients were treated with CWH for a total of 357 days. Estimated energy needs (2,408 ± 515 kcal / d) correlated well with measured energy needs (2,348 ± 706 kcal/d; r = 0 .78). The mean UAR was 13.2 ± 4 .7g N/d. There was no difference in mean UAR between patients receiving less than 1 .0 g versus 1 .0 g or more of protein/kg/d. The mean NND was - 8.3 ± 6.1 g N/d . Those patients receiving 1.0 g or more of protein/kg/d (n = 16) had a s g i nificantly lower NND than those patients who received less. Five patients receiving 1.0 g or more of protein/kg/d achieved a positive nitrogen balance. These patients had a nonprotein calorie-to-nitrogen ratio (132± 37) that was significantly less than that administered to patients who did not achieve a positive nitrogen balance (169 ± 33; P > 0 .05) . • Conclusions: Estimated energy expenditures using a modified Harris-Benedict equation provided moderate predictability with measured energy expenditures. The provision of 1 .0 g or more of protein/kg / d did not increase the UAR and was associated with a decreased NND. The provision of a lower nonprotein calorie-to-nitrogen ratio in patients receiving 1.0 g or more of protein/kg/d was associated with a positive nitrogen balance. © 1993 by the National Kidney Foundation, Inc.

*Renal Nutrition Specialist, Department of N utrition and Dietetics, In diana University Medical Center, n I dianapolis, IN. tRenal Nutrition Specialist, Departm ent of Nutrition and Dietetics, Indiana University Medical Center, Indianapolis, IN. tAssistant Professor, Section of Biostatistics, Dep artment of Public Health Sciences, Bowm an-Gray School of Medicine, Wins ton-Salem, NC. §Assistant Professor, Section of Nephrology, Department of Medicine, Indiana University Medical Center, Indianapolis, IN. Supported by a research g rant (EX91 06-06) from the Na tional Kidney Foundation 's Council on Renal N utrition. Address correspondence and reprint re quests to Mary H . Murphy, MS, RD, C NSD, c / oWilliam L. Ma cias, MD, PhD, 112 0 South Dr, Fesler H all, Rm 108, Indianap olis, IN 46202. © 1993 by the National Kidney Foundation, Inc.

1051 -2276 / 93 / 0302-0002$03.00 / 0 Journal of Renal Nutrition, Vol 3, No 2 (April), 1993: pp 67-74

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MURPHY ET AL

68

R

ECENT ADVANCES in continuous renal replacement therapies for critically ill patients with acute renal failure (ARF) have focused on increasing the urea clearance rate to provide improved control of metabolic waste products. 1 .2 However, improving the urea nitrogen clearance in these patients without understanding the magnitude of their urea appearance rates (UARs) or net nitrogen deficits (NNDs) may lead to severe protein depletion despite the ability to provide more aggressive nutritional support with these therapies. Previous studies have reported UARs ranging between 3.0 to 42.0 g nitrogen (N)/d in patients with ARF.3,4 This large degree of variability in UARs may reflect differences in both severity of illness among study patients and their degree of renal impairment. 4,5 Dissimilarity in the administered nutritional regimens (essential versus mixed amino acid preparations), as well as differences in the type and frequency of renal replacement therapy employed, also may have contributed to the wide range of reported UARs. These studies suggest that because of the high UARs in these patients, positive nitrogen balance cannot be obtained regardless of the nutritional regimen administered. 6 However, the nutritional regimens employed in these studies may not have been adequate to support this conclusion.7 The investigators studied a series of critically ill patients with ARF managed with continuous venovenous hemofiltration (CWH). The objectives of this investigation were to: (1) define the patient population demographics and the severity of illness; (2) quantify UARs in these patients and the magnitude of their NNDs; (3) compare estimated versus measured energy expenditures; and (4) compare the ability to meet nutritional needs with varied routes of nutritional support.

METHODS Patient Selection Patients with ARF receiving CWH at Indiana University Medical Center between June 1991 and June 1992 were eligible for inclu-

sion in this study. A nephrology consult was obtained before the initiation of CWH, and informed consent was obtained per institutional protocol. This was a noninteNentional study with prospectively collected data; therefore, no additional consent was indicated. Exempt status (no. EX91 06-06) was obtained through the Institutional Review Board.

Hemofiltration The standard operating protocol currently in place at Indiana University Medical Center 8 was observed for all patients undergoing CWH. The extracorporeal circuit was set up and changed every 48 hours by dialysis nurse personnel. The extracorporeal circuit was inspected daily and changed if clotting was present. The actual CWH procedure was performed by the intensive care nursing staff, who were responsible for monitoring the extracorporeal circuit, ultrafiltrate production, and calculating appropriate bicarbonate-based ultrafiltrate replacement rates. Replacement fluid was administered in a predilutional (prefilter) mode. The ultrafiltrate volume, necessary in calculating the UAR, was measured and recorded hourly. Serum chemistries were measured every 6 hours. Decisions regarding the nutritional support regimen and/or CWH parameters were not influenced by the investigators.

Data Collection Data, including patient weight, total fluid input, total fluid output, fluid composition, CWH parameters, nutritional support components, and laboratory data, were collected every 24 hours while the patient received CWH. The standard study day was considered to be 6:00 AM to 6:00 AM. An uninterrupted study day was defined as a 24-hour period during which CWH was discontinued for less than 60 minutes or the ultrafiltrate production rate was greater than 22 L. The severity of illness was assessed within the first 24 hours of admission to the intensive care unit and for each day of CWH therapy using the Acute Physiology

UAR AND NND IN PATIENTS RECEIVING CWH

69

and Chronic Health Evaluation (APACHE) II classification system. 9 * The amount and type of blood products administered were quantified for each day of CWH therapy. The nitrogen content of platelets and packed red blood cells was assumed to be 13.0 mg N/ml of administered blood product volume. 10 ,11 The nitrogen content of fresh frozen plasma also was assumed to be 13.0 mg N/m1.10 This latter value was confirmed by an analysis of 10 U of fresh frozen plasma by OA Laboratories and Research, Inc (Indianapolis, IN) using the microkjeldahl method. 12

value similar to that reported by Clark et aP5 in patients with ARF receiving CWH. The NND was estimated as the difference between dietary nitrogen intake and nitrogen output for each uninterrupted study day. The dietary nitrogen intake was calculated by review of the nutritional prescription, the actual administered volume, and the product information for parenteral and enteral amino acid/protein solutions .16 For those patients able to tolerate oral feedings, the nitrogen content of foods was calculated from values reported by Pennington. 17 Nitrogen output was the sum of the UFN and other nitrogen losses estimated as 4 g / dwhen stool loss was present and 2 g/ d when it was not. 18 Urinary urea nitrogen loss was considered to be negligible because all patients had ARF, and the majority (> 70%) had oliguria or anuria. In those patients who were nonoliguric, quantification of the 24-hour urinary nitrogen losses were conSistently less than 300 mg/d (281.3 ± 99 .3 mg/d; n = 25 collections from 6 patients). Nonurea nitrogen losses and the nitrogen content of blood products were not included in the calculation of the NND. Basal energy expenditure was estimated using the Harris-Benedict equation. 19 The ideal body weight was used if the patient was within 120% of the ideal body weight, and an adjusted body weight 20 was used if the patient's estimated dry weight was greater than 120% of ideal body weight. The basal energy expenditure was then modified by a standardized stress factor to achieve the estimated energy expenditure. Each patient's hospital course was reviewed for the presence of one or more of three previously identified stressors (sepsis, surgery, and malnutrition). which are known to increase energy needs. To achieve the overall estimated energy expenditure, the basal energy expenditure was multiplied by 1 .5 in the presence of one stressor, 1.7 in the presence of two stressors, and 1.9 in the presence of three stressors .

Indirect calorimetry was performed by the Vital Function Laboratory using an MMC Horizon System Metabolic Cart (Beckman Instruments, Inc, Anaheim, CA) . To prevent an underestimation of carbon dioxide production because of loss of carbon dioxide across the hemofilter, 13 measurements were completed only during the extracorporeal circuit change. All data were maintained in a computerized data base (Macintosh EXCEL, Apple, Cupertino, CA), which was specifically designed for this study. All calculations were done by computer.

Data Analysis The UAR was calculated for every uninterrupted study day using the formula UAR (g/24h)

+

=

UFN

(BUN2 - BUN1 x 0.6 x BW1)

+

(BW2 - BW1 x BUN2)

where UFN was the urea nitrogen loss across the hemofilter (g/24 h); BUN1 and BUN2 were the initial and ending blood urea nitrogen concentrations (g / L), respectively; and BW1 and BW2 were the initial and ending body weights (kg) , respectively.4,14 UFN was calculated as the volume of ultrafiltrate per day times the daily mean BUN concentration estimated by the fraction (BUN1 + BUN2)/2. The urea volume of distribution was assumed to be 0 .6 L/kg , a *The APACHE II uses a point score based on initial values of 12 physiological measurements, age, and chronic health status to provide a measure of severity of illness .

Statistical Analyses Descriptive statistics were used to summarize the patient population, CWH data,

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MURPHY ET AL

amount and type of nutrition received, UARs, and NNDs. At! results are reported as a mean ± standard deviation (SO) where the reported mean is the mean of patients' mean calculated across all study days. Student's t Test was used to compare ending APACHE II scores of survivors versus nonsurvivors and to evaluate the impact of varying protein intakes on the UAR and NND. A Spearman Rank Correlation Coefficient was used to quantify the relationship between estimated energy expenditure versus measured energy expenditure and to assess the relationship between blood product nitrogen and the UAR.

RESULTS Twenty-two men (age 52 ± 20 years) and 18 women (age 51 ± 19 years) were treated with CWH at the investigators ' institution between June 1991 and June 1992. The etiology of ARF was diverse (Table 1). Intubation and mechanical ventilation were required by 93% of patients. Vasopressor support was required by 83% of patients, 42% of which were categorized as requiring low-dose support « 10 ILg dopamine/kg/ min) ; 58% were categorized as requiring high-dose support (~ 10 ILg dopamine / kg / min and/or the addition of dobutamine or norepinephrine). Infection , defined as documented positive blood cultures, was present in 75% of patients . Ten patients (25%) survived their illness and were discharged from the hospital. TABLE 1. Etiology of ARF Primary Service

Event Preceding ARF

Medicine Hepatic failure (n = 16) Septic shock Cardiogenic shock Bone marrow transplantation Cardiothoracic postpump Surgery (n = 24) Organ tran splantation (4-liver, 1-kidney, 1-lung) Aortic aneurysm resection Pancreatic resection Cholecystectomy Transesophageal fistula Small bowel re sec tion Total

No. of Patients 6 4 2 4 9 6

3 2 2

40

Seven of the 10 survivors recovered lifesustaining renal function. The mean APACHE II score within 24 hours of admission to the intensive care unit was 25 ± 8.6 (range , 4 to 45). There was no difference in beginning APACHE II scores for survivors (24 ± 8 .6) versus nonsurvivors (26 ± 8.6; P > .50). As expected , survivors showed an improvement in their consecutive APACHE II scores and the final APACHE II score , obtained at discontinuation of hemofiltration, was significantly different from that of nonsurvivors (21 ± 7.2 versus 30 ± 6.1 ; P < .05). The primary indication for the selection of CWH over other renal replacement therapies was the presence of hypotension or excessive volume overload . The average duration of CWH therapy was 8.9 ± 8.6 days (range, 1 to 42; median, 5 days). The average ultrafiltrate production rate was 990 ± 63 mL/h. The mean weight loss from initiation to cessation of CWH was - 7.2 ± 6.7 kg (range, -21.8 to +3.4 kg). Adequate control of azotemia, defined as a BUN less than 40 mmol/L (110 mg/dL) , was achieved in all but one patient. Dietary nitrogen provided a mean of 9.3 ± 5.4 g/d (0.86 ± 0.48 g protein/kg/d). Mean nonprotein calorie administration was 1,697 ± 904 kcal/d (24 .0 ± 12.8 kcal/kg/ d), with a mean nonprotein calorie-tonitrogen ratio of 175:1. The mean proportion of substrate amounts provided were 29% fat and 71 % carbohydrate. Hyperglycemia, defined as a mean daily glucose greater than 15 mmol / L (250 mg / dL) , occurred in 40% of cases and was potentially influenced by one or more of the following factors: high-dose steroid administration, sepsis, rapid advancement of parenteral nutrition, and history of diabetes . Blood products were received by 93% of patients and provided a mean nitrogen load of 11.0 ± 15.3 g N/d (range, 0 to 56 g N/d). Paired data for individuals (one day receiving a blood product nitrogen load and one day receiving no blood product nitrogen) were matched for dietary nitrogen and total nonprotein calories received and showed no statistically significant relationship

71

UAR AND NND IN PATIENTS RECEIVING CWH

TABLE 2. Comparison of Routes of Nutritional Support and Relative Abilities to Meet Energy and Protein Needs Route of Nutritional Support Oral intake only Enteral nutrition only Enteral + parenteral Parenteral + oral Enteral + parenteral + oral Parenteral only No nutritional support

No. of Patients

Calories Provided (91,)* Estimated Needst 0

Protein Provided Protein Needed (%)

2 4 5

19 33 61 48 69 85

2 33 56 28

0

0

25 2

77

61

*Percentageswill not total 100% because of combination of feeding regimens. tEstimated needs based on modified Harris-Benedict equation per protocol.

(P > .20) between blood product nitrogen administration and the UAR. Of the 357 patient days, 205 met criteria for uninterrupted days. Only uninterrupted study days were used to calculate the UARs and NNDs. The mean UAR was 13.2 ± 4.7g/d (range, 5.1 to 22.4 g/d). The mean NND was -8.3 ± 6.1 g N/d (range, +6.7 to -20.8 g N/d). There was no difference in the mean UARs between patients receiving an average of 1.0 g or more of protein/kg/d (n = 16) compared with those receiving an average of less than 1.0 g protein/kg/d (n = 18); 13.7 ± 4.7 versus 13.0 ± 4.4; P > .50. * However, those patients who received an average of 1.0 g or more of protein/kg/d had a significantly lower NND compared with those patients who received less (P = .002), and 5 patients (31 %) achieved a mean positive net nitrogen balance. Of the 16 patients that received an average of 1.0 g or more of protein/kg/d, the protein administration rates for those achieving a positive nitrogen balance (1.3 ± 0.1 g/kg/d) were not different from those who remained in negative nitrogen balance (1.2 ± 0.2 g/kg/d; P > .05). The mean estimated energy expenditure was 2,408 ± 515 kcal/d (36 kcal/kg/d; range, 28 to 58). The mean measured energy expenditure (n = 10) was 2,348 ± 706 kcal/d (35 kcal/kg/d; range, 28 to 46), with a respiratory quotient of 0.86 ± 0.13. Estimated energy expenditure correlated

well with the measured value in those patients in whom the measured energy expenditure was obtained (r = 0.78). Patients who received an average of 1.0 g or more of protein/kg/d and achieved a positive nitrogen balance had a nonprotein calorie-tonitrogen ratio (132 ± 37) that was significantly different from that administered to patients who did not achieve a positive nitrogen balance (169 ± 33; P < .05). The route of nutritional support provided and the comparative ability to meet energy and protein needs are summarized in Table 2. Only 43% of patients met a minimum of 75% of their estimated energy needs. Parenteral nutrition alone provided the greatest consistency in maximizing nutritional support. Ten patients (25%) received some form of enteral support. However, multiple complications interfered with attempts to meet estimated energy and protein needs in 9 of these patients (Table 3). No specific enteral formula appeared more advantageous in providing successful nutritional support. Mean serum albumin was 31.0 ± 5.6 gil (3.1 ± 0.56; range, 2.2 to 3.8 g/dL). Use of this parameter for nutritional assessment was compromised by routine administration of exogenous albumin (93% of patients). The mean serum transferrin level was 1.57 ± 0.60 with a range of 0.39 to 2.91 gil (157 ± 60; median, 152 mg/dL), which indicated moderate to severe depletion of visceral proteins.

DISCUSSION *Those patients receiving less than 5 nonprotein kcal/kg/d and less than 0.1 g protein/kg/d were excluded from the analysis (n = 6).

The patient population had a significant mean UAR of 13.2 g N/d, which is similar to

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MURPHY ET AL

TABLE 3. Summary of Complications With Enteral Feedings, Feeding Tube Position, and Enteral Products Used Complications (n = 9) Excessive residuals Clogged / kinked tube Feeding Interruptions Diarrhea

No. of Patients

Tube Position

Enteral Feeding

5

NG-4, ND-1 NO , JT NO JT

Isocal ,* Jevity,t Pulmocare,t Suplena,t Vivonex:j: Magnacal§ Jevity, Pulmocare, Suplena Peptamenll, Tolerex:j:

2

Abbreviations : NG , nasogastric; NO , nasoduodenal ; JT, jejunostomy. *Mead Johnson, Evansville , IN. tRoss Laboratories, Columbus, OH. :j:Norwich Eaton, Norwich , NY. §Sherwood Medical, St Louis, MO. IIClintec, Deerfield, IL.

those previously reported 4 ,6 However, in these studies the severity of illness was not documented, and multiple renal replacement therapies were used in these patient populations. CWH provided adequate control of metabolic waste products and a predictably large ultrafiltrate production rate consistent with previous investigations,2,8 which allowed for nutritional support without fluid limitations, The considerable level of severity of illness (mean admission APACHE II score of 25) parallels the experience of Maher et al 21 and Forsberg et al. 22 The ability to make accurate comparisons and draw conclusions between study groups of different investigators is dependent on having an objective measure of severity of illness for patients with ARF, which is possible when the APACHE II classification system is applied. The mean NND (-8,3 g N/d) observed in this population is consistent with previously published data,4,6 yet it does not concur with conclusions by Feinstein et al 6 that provision of greater amounts of nitrogen increases the UAR without a significant improvement in the NND, Administration of 1.0 g or more of protein/kg/d appeared to reduce the degree of NND without increasing the UAR, which supports the preliminary findings of Talbot et al.7 The present study's patients who achieved a positive nitrogen balance appeared to do so primarily as a result of a reduced UAR. Factors that have been suggested to reduce the UAR in patients with ARF include increased nonprotein calorie-to-nitrogen ratio as well as re-

duced nitrogen administration,23-25 However, in the present investigation a lower nonprotein calorie-to-nitrogen ratio was associated with a lower UAR in those patients who received 1,0 g or more of protein/kg/d, These data imply that at higher protein administration rates (> 1,0 g protein/kg/d), an increase in the nonprotein calorie-tonitrogen ratio may not lower UARs as has been suggested to occur with lower levels of protein administration,4,23 Consequently, an improved understanding of the nutritional and nonnutritional factors that influence the UAR should be a major focus of future investigations. Paired data for individual patients showed no statistically significant relationship (P > .20) between blood product nitrogen administration and the UAR. These results support Feinstein's4 belief that this nitrogen should not be factored into the net nitrogen balance equation because blood components are replacing previous losses and are not immediately catabolized. Further investigation is needed to evaluate if a lag period exists from the time the blood products are administered and subsequently metabolized, which may allow the nitrogen load to impact the UAR at a later time. Estimated energy needs (2,408 ± 515 kcal/d) were calculated using a modification of the Harris-Benedict equation, For those patients in whom a measured energy expenditure was obtained (2,348 ± 706 kcal/d), there appeared to be good correlation with the estimated value (r = 0.78) and with previously reported values of 2,397 ±

UAR AND NND IN PATIENTS RECEIVING CWH

73

572 kcal / d 26 for patients with ARF. The predictive value of this modification of the Harris-Benedict equation was in contrast to previous reports that have questioned the accuracy and bias of the standard HarrisBenedict equation when applied to the critically ill patient. 27 ,28 A possible explanation for this discrepancy may be that a standardized weight as well as variable stress factors were used for each patient. However , the small sample size was insufficient to determine if these applied stress factors adequately quantified the multitude of stressors that impact the energy needs of patients with ARF. Consequently, the wide range of individual calorie requirements and concerns with overfeeding the ventilator-dependent patient support the use of indirect calorimetry to measure the energy needs in the acutely ill unless it is not available or not technically possible . Barriers to obtaining indirect calorimetry in the study population included a fractional inspired oxygen greater than 50%, air leak around tracheostomy, isolation precaution with bone marrow transplantation, patient refusal , and coordinating the time of the indirect calorimetry study with the extracorpo real circuit change . There is consensus in all areas of nutritional support literature that a functional gastrointestinal tract should be used to provide nutritional support when possible. However, the present data support the conclusion of Teschan et al 5 that 95% of patients with ARF cannot be fed adequately with enteral nutrition . The most common complication observed with enteral nutrition in the study population was excessive residuals , which was associated with nasogastric feeding tube placement 80% of the time. Transpyloric placement of the feeding tube may improve the chance of success with enteral feedings, yet the advancement of the feeding regimen to meet energy needs is still much slower compared with parenteral nutrition . The importance of expediting advancement of the feeding regimen to meet energy and protein needs is evident with the substantial NND accumulated each day without adequate nutrition. Although only 43% of patients met a minimum of 75%

of their estimated energy needs , this reflected the aggressiveness of the nutritional regimen ordered by the primary team , not necessarily the inability to tolerate the feeding regimen. Patients were potentially able to meet 100% of protein and calorie needs if the regimen was ordered as parenteral nutrition , and for one patient, as enteral nutrition. An optimal regimen may include the provision of small volumes of enteral nutrition to preserve gut integrity, if tolerated , and 100% of nutritional needs given parenterally.

CONCLUSIONS 1. This severely ill patient population w ith ARF demonstrated a significant mean UAR (13 .2 g N/d) that did not appear to be influenced by blood product nitrogen administration. 2. The provision of 1.0 g or more of protein/kg/d appeared to decrease the NND without increasing the UAR. However, achievement of a positive nitrogen balance seemed to be influenced more by the magnitude of the UAR rather than the amount of protein provided . 3. Estimated energy expenditure using the Harris-Benedict equation standardized for body weight and stress factors provided a moderate level of predictability with measured energy expenditure. This equation may be used when indirect calorimetry is not available or not technically possible. 4. In the study patients , parenteral nutritional support was better tolerated and advancement to meet energy and protein needs was faster compared with enteral nutrition . Parenteral nutrition should be the primary source of nutritional support in patients with ARF receiving CWH. 5. Future investigations should be prospective interventional study designs that evaluate the predictors of the UAR in patients with ARF, eg, APACHE II scores, clinical characteristics, and nutritional support regimen provided.

74

ACKNOWLEDGMENT The investigators than k Shawn Ostermann for his computer expe rtise in creating the customized data base and Gary McNally for the technical assistance in updating and maintaining the files .

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MURPHY ET AL 14. Blumenkrantz MJ , Kopple JD , Gutman RA, et al: Methods for assessing nutritional status of p atients with renal failure . Am J Clin Nutr 33:1567-1585 , 1980 15. Clark WR, Murphy MH , Alaka KJ , et al: Urea kinetics in continuou s hemotiltration. Trans Am Soc Artif Intern Organs 38M664-M667 , 1992 16. Olin BR (ed): Facts and Comparisons. St Louis, MO, Lippincott, 1992 17. Pennington JA (ed): Food Values of Portions Commonly Used. Philadelphia , PA, Lippincott , 1989 18. Alpers DH : Protein and calorie requirements , in Alpers DH , Clouse RE , Stenson WF (eds) : Manual of Nutritional Therapeutics. Boston, MA, Little, Brown, 1983, p 146 19. Blackburn GL. Bistrian BR, Maini BS , et al : Nutritional and metabolic assessment of the hospitalized patient. J Parenter Enter Nutr 1 :11-22, 1977 20. Wilkens K (ed): Suggested Guidelines for Nutritional Care of Renal Patients . Chicago, IL American Dietetic Association , 1986 21. Maher ER, Robinson KN , Scobie JE, et al: Prognosi s of critically-ill patients with acute renal failure : APACHE II score and other predictive factors . Q J Med 72:857-866 , 1989 22. Forsberg E, Soop M, Thorne A: Energyexpenditure and outcome in patients with multiple organ failure following abdominal surgery. Intens Care Med 17403-409, 1991 23. Spreiter SC, Myers BD, Swenson RS: Proteinenergy requirements in subjects with acute renal failure receiving intermittent hemodialysis. Am J Clin Nutr33 :1433-1437,1980 24. Miller RL, Taylor WR, Gentry W, et al: Indirect calorimetry in postoperative patients with acute renal failure. Am Surgeon 4 :494-499, 1983 25. Mault JR, Bartlett RH , Dec hert RE , et al: Starvation: A major contribution to mortality in acute renal fai lure? Trans Am Soc Artit Intern Organs 29:390-394, 1983 26. Bartlett RH, Mault JR, Dechert RE, et al: Continuous arteriovenous hemofiltration : Improved survival in surgical acute renal failure? Surgery 100400-407, 1986 27. Mann S, Westenkow DR, Houtchens BA: Measured and predicted calorie expenditure in the acutely ill. Crit Care Med 13: 173-1 77, 1985 28. Bartlett RH , Dechert RE , Mault, JR, et al: Measurement of metabolism in multiple organ failure. Surgery 92:771-778 , 1982