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Development of an index to assess the efficacy of nutritional support in gastrointestinal patients
CLINICAL
NUTRITION (1988) 7: 25-32 c Longman Group UK Ltd 1988
Development of an Index to Assess the Efficacy of Nutritional Support in Gastrointestinal Patients J. Comes, B. Garel, H. Tello, D. Evard, P. Baumer, J. P. Gendre, M. Le Quintrec and Y. Le Quintrec Service de Gastroentkrologie et de pathologie digestive post-opkratoire, 75571 Paris cedex 12, France (Reprint requests to J.C.)
HBpital Rothschild,
33 Bd de Picpus,
This study was conducted to develop an index of the overall efficacy of a nutritional support program in gastrointestinal patients. Eighteen nutritional parameters were recorded in 200 consecutive patients before and after a 25day nutritional support. Multiple regression analysis was performed using the patient’s clinical change as dependent variable and the 25day deltas of each parameter as independent variables. The data from the 100 first patients were used to select among the 18 parameters the best indicators of the nutritional change, the data from the 50 following patients were used to define the index, and the last group was used for validation of the index. The composite index obtained from analysis included eight parameters, in decreasing order of contributive value: serum-albumin, body-weight, spontaneous oral intake, creatinine-height index, triceps skin fold, serum transferrin, mid-arm muscle circumference, and hemoglobin. In the last 50 patients, the value of the index was closely related to an independent appraisal of the patient’s clinical change. Sensibility and specificity of the index to recognise nutritionally improved patients from the remaining, and worsened patients from the remaining, were 96% and 8 1 y/,, and loon+, and loo%, respectively. This therapeutic index would permit an objective quantitative assessment of the nutritional response to enteral or parenteral support and would allow comparisons of various nutritional regimens applied to gastrointestinal patients.
ABSTRACT
INTRODUCTION
the specific effect of the nutritional therapeutics, i.e., the nutritional change of the patient. The objective of this prospective study was then to develop an index of the overall efficacy of a nutritional support program in gastrointestinal patients. We believed that such an index should satisfy the following requirements: a) it should incorporate factors considered by most nutritionists and gastroenterologists to be reliable, economic, and easy to collect, indicators of nutritional status; b) it must demonstrate exclusively the normalisation of nutritional parameters and must be independent from over-nutrition, as the goal of a therapeutic program must be only to correct malnutrition, and not to achieve obesity or biological supranormal values; c) it should be independent from the disease process accountable to malnutrition; d) it should demonstrate accurately the overall change of the nutritional status of an individual patient, having a positive value when nutritional status improved, and a negative value when nutritional status worsened; e) it should require only relatively simple computations. The present paper reports the development of such an index.
Malnutrition is frequent in patients with gastrointestinal disease and has led to a considerable interest for methods of nutritional support as total parenteral nutrition [I, 21 or continuous enteral nutrition [3,4]. Numerous scoring systems have been proposed to assess nutritional status [5-71. These index, although accurate to predict operative morbidity and mortality in a group of patients [6-91, cannot be used to document how much the nutritional status of a patient receiving nutritional support does improve, or deteriorate. This evaluation is currently based on the changes of the clinical condition of the patient. However such a clinical evaluation is very dependent on the observer and his own experience [ 10,l l] and cannot be used to compare various nutritional therapeutic regimens because it lacks objective criteria. In addition, intra-individual cross-over comparisons cannot be performed as the nutritional status of a patient changes slowly, and the result obtained from a first regimen may influence the response to a second one. Thus, to allow the objective comparison of various nutritional support regimens [ 121, there is a need for an index which could quantify 25
26
DEVELOPMENT
OF AN INDEX TO ASSESS THE EFFICACY
OF NUTRITIONAL
SUPPORT
IN GASTROINTESTINAL
PATIENTS
Table 1 Patients Phase 1 (n = 100) Phase 2 (n = 50) Phase 3 (n = 50) Age (yr, mean * SD) Men/women Diagnosis: Without intestinal disease:
Malabsorption
Inflammatory
syndromes:
bowel diseases:
-Benign oesogastric aesogastric cancer -Gastric resection --Pancreatitis -Anorexia -Short bowel -Coeliac disease -Miscellaneous -Ulcerative colitis -Crohn’s disease -Radiation enteritis
disorders
Nutritional support: Continuous enteral nutrition Total parenteral nutrition
PATIENTS
AND METHODS
study was carried out into three consecutive phases. Phase 1 was to define and to select the independent variables of the index. Phase 2 led to the final development of the index. Phase 3 was for validation of the index.
48.5 f 18.1 48/52
47.2 f 18.8 21/29
46.5 f 19.2 26/24
5 9
11 9 6 19 4 4 5 6 12
2 3 6 1 1 10 0 3 0 20 4
3 0 4 3 3 11 0 2 16 7
88 12
46 4
45 5
1
method of nutritional support of the patients from the three series.
The
Patients Three consecutive series of patients were studied: from January 1981 to August 1983, patients no l-100 (phase 1); from September 1983 to October 1984, patients nn 101-150 (phase 2); from November 1984 to December 1985, patients n” 151-200 (phase 3). All those patients had been referred to us for nutritional management and they did receive nutritional support, either continuous enteral nutrition, parenteral nutrition, or both. Nutritional support was maintained for at least 10 days, and the patient was maintained in hospital for at least 22 days after nutritional therapy was started. We excluded the patients whose day 25 assessment was not available because during this interval they died (three patients), had to be operated upon (seven patients), or were discharged (10 patients). The patients were classified into three groups according to the presence and the nature of intestinal disease: chronic malabsorption syndrome (CMS), inflammatory bowel disease (IBD), and without intestinal disease (WID). A few patients with mixed disorders were classified according to the dominant feature at the time the study was conducted. The interval between intestinal surgery and inclusion to the study exceeded 3 weeks in all patients. Table 1 gives the age, sex, diagnosis, and
Nutritional assessment Each individual patient was studied prospectively the day before starting the nutritional support (day 0) and 3-4 weeks thereafter (day 25). This interval was chosen because previous longitudinal studies suggested that a 3-wk therapeutic period was necessary to achieve a significant nutritional improvement [3]. Sixteen nutritional parameters were measured (Table 2). Triceps skinfold thickness was measured to the nearest 0.1 mm with the Harpenden caliper (John Bull, Liverpool). The reading was made on the mid point from elbow to acromia of the non-dominant arm, with the subject sitting in a relaxed condition. Mid-arm circumference was measured at the nearest mm, and arm-muscle circumference was determined by the formula of Blackburn et al [13]. The patient was weighed and the presence or absence of edema was noted. All these measurements were performed by the same of us (MLQ). Basal blood samples and 24h urine were collected the same day. Serum albumin was determined by gel electrophoresis and serum transferrin by radial immunodiffusion. Spontaneous oral caloric intake (the 24h total caloric intake the patient was ingested by mouth, whatever he was receiving calories by vein or gastric tube) was evaluated by examination of the remaining foods from the meals. Body weight was expressed as percentage of ideal for sex and height [13] and 24h urinary creatinine as creatinine-height index according to the tables from Blackburn et al [ 131. Spontaneous oral caloric intake
CLINICAL
Table 2
Nutritional
parameters Number
Parameter
x1 x2 x3 x1 x< x6 X3
xa x9 x1,, x11 x1: x11 x14 x1\ xlh
27
NUTRITION
Threshold
Item
Body weight as a percent of ideal body weight Triceps skin fold Mid-arm muscle circumference Creatinine-height index Daily oral caloric intake Serum albumin Serum transferrin Hemoglobin Serum cholesterol Body weight as a percent of BW 3 mo. before Total lymphocyte count Serum magnesium Abnormal alkaline phosphates and/or ASAT Urinary sodium Urinary potassium Edema
of subnormal
values’
value
90”,, M,,, 11.2 mm/W, 14.8 mm M, 22.8 cm/W, 20.9 cm 90 ci<, 30 kcal/IBW kg 3.50 g/d1 200 mg/dl M, 13 g/dl/W, 12 g/d1 4.00 mmol/l 95”,, 1200 /mm’ 0.70 mmolil 50 mzzlj24 40 mmol/24 absent
h h
Day 0
Day 25
89 91 83 88 85 78 47 64 59 78 35 47 25 52 44 17
84 87 75 75 72 69 ‘2 73 49 30 25 38 17 26 22 13
a number of patients (from 100) with xi value under threshold. b Abbreviations: BW, body weight; M, men; W, women.
was expressed body weight.
Description
as the daily
number
of kcal per kg of ideal
of phase 1
Phase 1 analysis was performed to define and select the most reliable and contributive independent variables of the index. To achieve this goal, the following steps were taken: a) the nutritional parameters which in the present series had a normal value on day 0 in most patients, or which had mean values significantly different from a diagnostic group to another, were first deleted; b) the independent variables were defined as the 25day deltas of each selected parameter, Ax, = (xIDIS- xi,&; an important objective was to fulfil requirement (b), independence of the index from overnutrition. To achieve this, we determined for each nutritional parameter a threshold value which corresponds to the lowest value of normal (Table 2). The deltas which were retained finally as independent variables were the only variations inside the pathological area (under threshold): any day 0 or 25 value above threshold was assigned = threshold and delta was not calculated when the day 0 and day 25 were both above threshold; c) the final step was a multiple regression analysis using y (over-all estimation of the nutritional change) as dependent variable [14]. The independent variables Ax, which had a low contributory value to y were then deleted. The contributory value of each variable to y was taken as the standard deviation of that variable times the coefficient b, and divided by the sum of such products for the n independent variables.
The dependent variable y for each patient n l-100 was the result of two physicians’ (JC and JPG) over-all evaluation of ‘how the patient’s nutritional status did improve, or worsen, from day 0 to day 25’. This evaluation was made blindly, taking into account the results of both clinical examination and nutritional measurements, and specified three grades: ‘better’, ‘the same’, and ‘worse’. On day 25 compared to day 0, 61 patients were found ‘better’ from the two evaluations, 13 patients were found ‘better’ from one and ‘the same’ from the other, 17 patients ‘the same’ from the two evaluations, two patients ‘the same’ from one and ‘worse’ from the other, and seven patients ‘worse’ from the two evaluations. The respective numerical values assigned to these five descriptions were + 8, + 3,0, - 2, and -7.
Description
of phase 2
The goal of phase 2 was the development of the coefficients of each selected independent variable of the index. The calculations reproduced exactly the final step of phase 1, but with a reduced number of independent variables and a redefined continuous dependent variable y. The limitations of phase 1 analysis resulted from that the individual parametric data were known when assessing y, that y could only take five arbitrary numerical values, and there was some interobserver disagreement. Particularly, we noticed that some patients with a slight nutritional improvement were very difficult to classify between ‘the same’ and ‘better’. The y value of patients n” 101-150 was then
28
DEVELOPMENT
OF AN INDEX TO ASSESS THE EFFICACY
OF NUTRITIONAL
determined in the following way: on day 0 and day 25, a clinical examination was performed by a physician unaware of the patient’s diagnosis, treatment, and nutritional assessment data (JPG for the patients receiving care from JC, and vice-versa). Several items (physical and intellectual activities, fatigability, behavior, facies, skin, hair, mouth and muscle appearance) were scored by using different scales as published elsewhere [15]. By comparing the changes of the items from day O-25, the physician quantified how about the patient’s nutritional status improved (from 0 to + 10) or worsened (from 0 to - 10) during the 25-day interval. Thus y was a continuous variable from - 10 to + 10.
Description
of phase 3
The index resulting from phase 2 computations was validated prospectively using a linear regression model relating the individual values of the index to y collected according to phase 2. In addition, the individual values of the index were calculated retrospectively in patients YZ’I-100. In the three consecutive groups of patients, the mean values of the index in patients with clearly improved (y > + 3), not significantly changed ( - 4 < y < + 4), and worsened (y < - 3) nutritional status, respectively, were calculated. After determining in patients no 101-150 the cut-off values of the index to recognise clearly improved patients from the remaining, and clearly worsened patients from the remaining, respectively, the number of true positive, true negative, false positive, and false negative inside each consecutive group of patients, and inside the whole group, was calculated and respective sensitivity, specificity, positive accuracy, and negative accuracy of the index to assess clinical nutritional improvement, and deterioration, were obtained.
Calcutations
The analysis of the data was done at the CICG of Grenoble (France) using its H Bull DPS 8/70 computer and programs SPAD and BMDP.
RESULTS Phase 1 (Selection
of the independent
variables)
The parameters xl1 (total lymphocyte count), x,~ (alkaline phosphatases and/or transaminases), and xl6 (edema) were normal on day 0 in most cases (Table 2). They were first dropped. The parameters xi2 (serum magnesium), xIp (urinary sodium), and x,~ (urinary potassium) were significantly more frequently sub-
SUPPORT
IN GASTROINTESTINAL
PATIENTS
normal in patients with intestinal disease (groups CMS and IBD) compared to patients from group WID; we thought then that their incorporation into the next calculations would introduce differences between the groups of patients and they were deleted. Multiple regression analysis with ax,, CI,x2, . . . , Lx,,) as independent variables obtained an encouraging result as multiple R was 0.789 with a F ratio of 13.82. variable Ax,,, (delta of body weight However, expressed as a percent of body weight 3 months before) was associated with a negative sign, and variable Ax, (data cholesterol) had a low fractional contributive value, less than 3”,, . These two variables were deleted. As a result of computations performed in patients n’ l-100, the number of independent variables was thus reduced from the initial 16 to eight.
Phase 2 (Derivation
of the index)
Patients n” 101-150 were very similar to patients n l-100 (Table 1) except that Crohn’s disease was a more frequent diagnosis. This was related to a changing therapeutic approach of patients with Crohn’s disease during recent years. The numbers of day 0 and day 25 xi subnormal values did not differ significantly from those of patients n” l-100. Multiple regression analysis with n x,, n x2, . . , A xg as independent variables led to the index indicated in Table 3. Multiple R was 0.935 with a F ratio of 35.64. Each of the raw coefficients was divided by the smallest one (that of x,) to give standardised coefficients. Values were then rounded to the nearest decade as shown in Table 3. The rounded coefficients are the final ones used for calculating the index. Table 4 gives an example of calculation of the index in one individual patient, and Figure 1 illustrates the card used to collect data and to facilitate computation of the index. Figure 2 gives the regression of the individual values of the index in the patients n’ 101-150. Regression slopes in WID, CMS, and IBD patients, were not significantly different.
Phase 3 (Validation
of the index)
Figure 3 gives the regression of the individual values of the index in the patients n” 151-200. The values of the index were highly related to the clinical evaluation (r =0.86, p
CLINICAL
Table
Derivation
3
of the index
Variable
Item
Delta Delta Delta Delta Delta Delta Delta Delta
Body weight (“” of IBW’) Triceps skin fold (mm) Muscle circumference (cm) Creatinine-height index (“,,) Oral intake (kcal.IBW kg *.d *) Serum albumin (g/d]) Serum transferrin Hemoglobin (g/dl)
x, x2 x3 x4 xs x6 x, xg
29
NUTRITION
Raw coefficient
Standard error
0.22243 0.43961 0.35869 0.02955 0.09639 2.86680 0.01173 0.18131
0.06037 0.19539 0.24943 0.00797 0.02249 0.50630 0.00655 0.14645
Standardised coefficient
Rounded coefficient
“,, contribution 20
70 140 120 10 30 1000 ‘t 60
75.3 148.8 121.4 10.0 32.6 970.2 4.0 61.4
10 6 12
14 25 7 5
a IBW, ideal body weight.
Table
Example
4
for calculation
MB, male, 20-year-old,
of the index
Ileocolonic
Crohn’s
disease
169 cm Ideal body weight
65.9 kg Ideal urinary
creatinine
Day 25
Day 0
Delta Observed value xl x1 x1 x4 x, x, x-
XX
Corrected value
The index
day
EODY WEIGHT
(% of
IBw)
FOLD
(n-m)
SKIN
MI D-ARM MUSCLE CIRCUMFERENCE SPONTANEOUS oRAL lNTAKE
‘cm)
ca I . IBW kg-’
CREATININE-HEIGHT
SERUM ALBUMIN
INDEX
(g/l00
49 kg = 74.4”,, 5.2 mm 20.0 cm 8.9 mmol= 70”,, 2850 kcal= 43.2 3.65 g/d1 225 mg/dl 12.6 g/d1
74.4 5.2 20.0 70 30.0 3.50 200 12.6
(mg/lOO
HEMOGLOBIN
ml)
Format
(g/l00
25
xI
un
:
+854 +140 + 228 ~ 30 + 672 + 580 ‘, 24
meanwiirr-7)
t 346
delta
wI x
70
11.2 14.8
I I I
x
140
male female
22.8 20.9
I I 1
x
120
.day-’
(I,
30.0
I 1I I
x
30
90.0
I I I
x
10
3.50
ml)
for hand calculation
day
0
200 male female
13.0 12.0
1 I 1I I III I III 1
of the index. The value of the index is mean w,
w,
+ 12.2 x 70 +1.0x140 + 1.9 X 120 -3x10 +22.4x 30 +0.58x 1000 not calculated -0.4 x 60
male female
ml)
SERUM TRANSFERRIN
Fig. 1
90.0
xI
x
Corrected value
-
THRESl-UJLD VALUE
TRICEPS
Observed value
62.2 4.2 18.1 73 7.6 2.92 200 13.0
41 kg=62.2”,, 4.2 mm 18.1 cm 9.4 mm01 = 73”,, 500 kcal= 7.6 2.92 g/d1 212 mg/dl 13.2 g/d1
Body weight Triceps skin fold Muscle circumference Urinary creatinine Oral intake Serum albumin Serum transferrin Hemoglobin
12.80 mmolj24
x
1000
X
4
x
60
l-7-n-l
h.
30
DEVELOPMENT
OF AN INDEX TO ASSESS THE EFFICACY
.4 clinical
OF NUTRITIONAL
SUPPORT
IN GASTROINTESTINAL
PATIENTS
-8 assessment
clinical
t
assessment
0
1
Fig. 2 Relation of the index to physician’s appraisal of the over-all nutritional change in patients n 101-150 (Phase 2, development of the index). Squares: WID patients; triangles: CMS patients; circles: IBD patients. and a specificity of 81 O0 for nutritional improvement, and sensitivity and specificity of loo”, for nutritional deterioration. Table 5 gives the statistical results of the index in the three consecutive groups of patients, and in the whole group of 200 patients. The mean values of the index in patients with improved, unchanged, and worsened nutritional status, were not significantly different from one phase to another. The overall accuracy of the index to assess nutritional improvement and deterioration was satisfactory in each phase as in the whole group. 96’,
DISCUSSION This prospective study developed an index which permits objective quantitative assessment of the nutritional response of a 2%day nutritional support in
Fig. 3 Relation of the index to physician’s appraisal of the over-all nutritional change in patients n” 151-200 (Phase 3, validation of the index). Regression slope was Index = 30.43 + 11 (n = 50, r = 0.86, p <: 0.001). Same symbols as Figure 2.
gastro-intestinal patients. The index fulfilled the five requirements we considered important. Furthermore, application of the index in a group of 50 patients who were not used to generate the equation showed that this index was an accurate numerical expression of the overall nutritional change of an individual patient receiving nutritional support. The parameters which were selected from analysis to enter the index were for the most, expected. It is noteworthy that two parameters which are considered universal and basic indicators of nutritional status, body weight and serum-albumin, were found to account for 459: of the index value (Table 3). This high contributive value could be related to the inverse relationship between the deltas of these two parameters when nutritional status did not change clearly in one patient: if body weight increased because of a gain of water, serum-albumin would fall; conversely, dehyd-
CLINICAL
31
NUTRITION
Table 5
Mean f SD, sensitivity, specificity, and positive and negative accuracy of the index to assess nutritional improvement and deterioration.
Patients N l-100 (Phase 1) N 101-150 (Phase 2) N 151-200 (Phase 3) N l-200
Mean * standard deviation improved unchanged worsened +218 f 125 (n=61) +206 f 101 (n=24) +168&69 (n = 24) +204 zr 108 (n= 109)
+48+82 (n=32) +49*70 (n=23) +51 f69 (n=24) +49+ 73 (n=79)
-113f97 (n= 7) -183f45 (n=3) -149 * 12 (n=2) -136i84 (n= 12)
Improved nutritional status? Se Sp PA NA
Worsened nutritional statusb Se Sp PA NA
85
77
85
77
71
97
62
98
87
77
78
87
100
98
75
100
96
81
82
95
100
100
100
100
88
78
83
85
83
98
71
99
n The cut-off value of the index to discriminate improved patients from the remaining was + 100. b The cut-off value of the index to discriminate worsened patients from the remaining was ~ 75. ration could be associated with high serum albumin but would produce a loss of weight; thus an improvement of both body weight and serum-albumin must indicate an improved nutritional status. Likewise, the value of mid-arm muscle circumference is in part negatively related to that of triceps skin fold, and during nutritional recovery, iron deficiency may lead to increased serum transferrin but with decreasing haemoglobin [ 161. Thus, six of the parameters entering the index are linked together in such a way that both improved values indicate necessarily a real improvement. Although it is clear that one nutritional parameter, taken separately, would correlate poorly with tissue repletion [17], this may be not true for a composite index [12]. Finally, a composite index has the capacity to take into account different independent items: the changes of body composition (fat, water, muscle and visceral protein) and the changes in individual capacities of nutritional recovery (caloric intake). However, one may notice that the index does not take into account the patient’s immunological functions, although those are considered as closely related to the nutritional status. The lymphocyte count was normal in most patients before the nutritional support program and thus could not be used as a valuable marker. Skin testing was not performed in this study because we had thought it was an expensive and time-consuming method, and anergy may be induced by extra-nutritional factors [18, 191. An important requirement of the index as a therapeutic index was to demonstrate exclusively the correction of deficiencies and not any over-correction. To fulfill this requirement, it was necessary to develop a relatively complex index, by deleting any supra-normal values. Such a complexity may be a limitation to further utilisation of the index. However, the use of a format (Figure 1) and experience render simple and fast the computations. Finally, the main usefulness of the index would be to allow the objective comparison of different therapeutic nutritional programs, inside a medical unit, and eventually in pluricentric studies.
REFERENCE
[l] Greenberg G R, Jeejeebhoy K N 1979 Intravenous protein-sparing therapy in patients with gastrointestinal disease. Journal of Parenteral and Enteral Nutrition 3: 427-432 [2] Matuchansky C, Morichau-Bauchant M, Druart F, Tapin J 1981 Cyclic (nocturnal) total parenteral nutrition in hospitalized adult patients with severe digestive diseases. Gastroenterology 81: 433-437 [3] Cosnes J, Tello H, Le Quintrec M et al 1983 L’alimentation enterale continue corrige-t-elle la denutrition des affection digestives? Resultats de l’etude longitudinale de 92 malades consecutifs trait& pendant trois h sept semaines. Gastroenterologie Clinique et Biologique 7: 1003-1009 [4] Morin C L, Roulet M, Roy C C, Weber A 1980 Continuous elemental enteral alimentation in children with Crohn’s disease and growth failure. Gastroenterology 79: 1205-1210 [5] Bistrian B R, Blackburn G L, Sherman M 1975 Therapeutic index of nutritional depletion in hospitalized patients. Surgery Gynecology Obstetrics 141: 512-516 [6] Buzby G P, Mullen J L, Matthews D C, Hobbs C L, Rosato E F 1980 Prognostic nutritional index in gastrointestinal surgery. American Journal of Surgery 139: 160-167 [7] Di Costanzo J, Martin J, Cano N et al 1983 Indice nutritionnel pronostique en chirurgie digestive. Gastroenterologie Clinique et Biologique 7: 851-856 [8] Ryan J A Jr, Taft D A 1981 Preoperative nutritional assessment does not predict morbidity and mortality in abdominal operations. Surgical Forum 31: 96-98 [9] Turner W W, Landreneau R J, Toler G F et al 1982 How accurate is nutritional risk classification? Surgical Forum 33: 107-109 [lo] Woolfson AM J 1983 Artificial nutrition in hospital. British Medical Journal 287: 1004-1006 [ll] Baker P B, Detsky A S, Wesson D E et al 1982 Nutritional assessment. A comparison of clinical judgment and objective measurements. New England Journal of Medicine 306: 969-972 [12] Cooper A, Heird W C 1982 Nutritional assessment of the pediatric patient including the low birth weight infant. American Journal of Clinical Nutrition 35: 1132-l 141 [ 131 Blackbum G L, Bistrian B R, Maint B S, Schlamm H T, Smith M F 1977 Nutritional and metabolic assessment of
32
DEVELOPMENT
OF AN INDEX
TO ASSESS
THE
EFFICACY
the hospitalized patient. Journal of Parenteral and Enteral Nutrition 1: 1 l-23 [ 141 Gunst R F, Mason R L 1980 Regression analysis and its applications, Marcel Dekker INC, New York [ 151 Cosnes J, Baumer P, Tello H et al 1987 Aide a la decision d’assistance nutritionnelle au tours des affections digestives chroniques. Gastroentirologie Clinique et Biologique 11: 201-205 [ 161 Delpeuch F, Cornu A, Chevalier P 1980 The effect of iron deficiency anemia on two indices of nutritional status, prealbumin and transferrin. British Journal of Nutrition 43: 385-379 Submission dare: 14 January
1986. Accepted: 18 June 1987
OF NUTRITIONAL
SUPPORT
IN GASTROINTESTINAL
PATIENTS
[ 171 Jeejeebhoy K N, Baker J P, Wolman S L et al 1982 Critical evaluation of the role of clinical assessment and body composition studies in patients with malnutrition and after total parenteral nutrition. American Journal of Clinical Nutrition 35: 1117-l 127 [ 181 McLaughlin G A, Wu A V, Saporoschetz I et al 1979 Correlation between anergy and a circulating immunosuppressive factor following major surgical trauma. Annals of Surgery 190: 297-304 [ 191 Meakins J L, Christou N U, Shizgal H M, McLean L D 1979 Therapeutic approaches to anergy in surgical patients. Annals of Surgery 190: 286296
NUTRITION (1988) 7: 25-32 c Longman Group UK Ltd 1988
Development of an Index to Assess the Efficacy of Nutritional Support in Gastrointestinal Patients J. Comes, B. Garel, H. Tello, D. Evard, P. Baumer, J. P. Gendre, M. Le Quintrec and Y. Le Quintrec Service de Gastroentkrologie et de pathologie digestive post-opkratoire, 75571 Paris cedex 12, France (Reprint requests to J.C.)
HBpital Rothschild,
33 Bd de Picpus,
This study was conducted to develop an index of the overall efficacy of a nutritional support program in gastrointestinal patients. Eighteen nutritional parameters were recorded in 200 consecutive patients before and after a 25day nutritional support. Multiple regression analysis was performed using the patient’s clinical change as dependent variable and the 25day deltas of each parameter as independent variables. The data from the 100 first patients were used to select among the 18 parameters the best indicators of the nutritional change, the data from the 50 following patients were used to define the index, and the last group was used for validation of the index. The composite index obtained from analysis included eight parameters, in decreasing order of contributive value: serum-albumin, body-weight, spontaneous oral intake, creatinine-height index, triceps skin fold, serum transferrin, mid-arm muscle circumference, and hemoglobin. In the last 50 patients, the value of the index was closely related to an independent appraisal of the patient’s clinical change. Sensibility and specificity of the index to recognise nutritionally improved patients from the remaining, and worsened patients from the remaining, were 96% and 8 1 y/,, and loon+, and loo%, respectively. This therapeutic index would permit an objective quantitative assessment of the nutritional response to enteral or parenteral support and would allow comparisons of various nutritional regimens applied to gastrointestinal patients.
ABSTRACT
INTRODUCTION
the specific effect of the nutritional therapeutics, i.e., the nutritional change of the patient. The objective of this prospective study was then to develop an index of the overall efficacy of a nutritional support program in gastrointestinal patients. We believed that such an index should satisfy the following requirements: a) it should incorporate factors considered by most nutritionists and gastroenterologists to be reliable, economic, and easy to collect, indicators of nutritional status; b) it must demonstrate exclusively the normalisation of nutritional parameters and must be independent from over-nutrition, as the goal of a therapeutic program must be only to correct malnutrition, and not to achieve obesity or biological supranormal values; c) it should be independent from the disease process accountable to malnutrition; d) it should demonstrate accurately the overall change of the nutritional status of an individual patient, having a positive value when nutritional status improved, and a negative value when nutritional status worsened; e) it should require only relatively simple computations. The present paper reports the development of such an index.
Malnutrition is frequent in patients with gastrointestinal disease and has led to a considerable interest for methods of nutritional support as total parenteral nutrition [I, 21 or continuous enteral nutrition [3,4]. Numerous scoring systems have been proposed to assess nutritional status [5-71. These index, although accurate to predict operative morbidity and mortality in a group of patients [6-91, cannot be used to document how much the nutritional status of a patient receiving nutritional support does improve, or deteriorate. This evaluation is currently based on the changes of the clinical condition of the patient. However such a clinical evaluation is very dependent on the observer and his own experience [ 10,l l] and cannot be used to compare various nutritional therapeutic regimens because it lacks objective criteria. In addition, intra-individual cross-over comparisons cannot be performed as the nutritional status of a patient changes slowly, and the result obtained from a first regimen may influence the response to a second one. Thus, to allow the objective comparison of various nutritional support regimens [ 121, there is a need for an index which could quantify 25
26
DEVELOPMENT
OF AN INDEX TO ASSESS THE EFFICACY
OF NUTRITIONAL
SUPPORT
IN GASTROINTESTINAL
PATIENTS
Table 1 Patients Phase 1 (n = 100) Phase 2 (n = 50) Phase 3 (n = 50) Age (yr, mean * SD) Men/women Diagnosis: Without intestinal disease:
Malabsorption
Inflammatory
syndromes:
bowel diseases:
-Benign oesogastric aesogastric cancer -Gastric resection --Pancreatitis -Anorexia -Short bowel -Coeliac disease -Miscellaneous -Ulcerative colitis -Crohn’s disease -Radiation enteritis
disorders
Nutritional support: Continuous enteral nutrition Total parenteral nutrition
PATIENTS
AND METHODS
study was carried out into three consecutive phases. Phase 1 was to define and to select the independent variables of the index. Phase 2 led to the final development of the index. Phase 3 was for validation of the index.
48.5 f 18.1 48/52
47.2 f 18.8 21/29
46.5 f 19.2 26/24
5 9
11 9 6 19 4 4 5 6 12
2 3 6 1 1 10 0 3 0 20 4
3 0 4 3 3 11 0 2 16 7
88 12
46 4
45 5
1
method of nutritional support of the patients from the three series.
The
Patients Three consecutive series of patients were studied: from January 1981 to August 1983, patients no l-100 (phase 1); from September 1983 to October 1984, patients nn 101-150 (phase 2); from November 1984 to December 1985, patients n” 151-200 (phase 3). All those patients had been referred to us for nutritional management and they did receive nutritional support, either continuous enteral nutrition, parenteral nutrition, or both. Nutritional support was maintained for at least 10 days, and the patient was maintained in hospital for at least 22 days after nutritional therapy was started. We excluded the patients whose day 25 assessment was not available because during this interval they died (three patients), had to be operated upon (seven patients), or were discharged (10 patients). The patients were classified into three groups according to the presence and the nature of intestinal disease: chronic malabsorption syndrome (CMS), inflammatory bowel disease (IBD), and without intestinal disease (WID). A few patients with mixed disorders were classified according to the dominant feature at the time the study was conducted. The interval between intestinal surgery and inclusion to the study exceeded 3 weeks in all patients. Table 1 gives the age, sex, diagnosis, and
Nutritional assessment Each individual patient was studied prospectively the day before starting the nutritional support (day 0) and 3-4 weeks thereafter (day 25). This interval was chosen because previous longitudinal studies suggested that a 3-wk therapeutic period was necessary to achieve a significant nutritional improvement [3]. Sixteen nutritional parameters were measured (Table 2). Triceps skinfold thickness was measured to the nearest 0.1 mm with the Harpenden caliper (John Bull, Liverpool). The reading was made on the mid point from elbow to acromia of the non-dominant arm, with the subject sitting in a relaxed condition. Mid-arm circumference was measured at the nearest mm, and arm-muscle circumference was determined by the formula of Blackburn et al [13]. The patient was weighed and the presence or absence of edema was noted. All these measurements were performed by the same of us (MLQ). Basal blood samples and 24h urine were collected the same day. Serum albumin was determined by gel electrophoresis and serum transferrin by radial immunodiffusion. Spontaneous oral caloric intake (the 24h total caloric intake the patient was ingested by mouth, whatever he was receiving calories by vein or gastric tube) was evaluated by examination of the remaining foods from the meals. Body weight was expressed as percentage of ideal for sex and height [13] and 24h urinary creatinine as creatinine-height index according to the tables from Blackburn et al [ 131. Spontaneous oral caloric intake
CLINICAL
Table 2
Nutritional
parameters Number
Parameter
x1 x2 x3 x1 x< x6 X3
xa x9 x1,, x11 x1: x11 x14 x1\ xlh
27
NUTRITION
Threshold
Item
Body weight as a percent of ideal body weight Triceps skin fold Mid-arm muscle circumference Creatinine-height index Daily oral caloric intake Serum albumin Serum transferrin Hemoglobin Serum cholesterol Body weight as a percent of BW 3 mo. before Total lymphocyte count Serum magnesium Abnormal alkaline phosphates and/or ASAT Urinary sodium Urinary potassium Edema
of subnormal
values’
value
90”,, M,,, 11.2 mm/W, 14.8 mm M, 22.8 cm/W, 20.9 cm 90 ci<, 30 kcal/IBW kg 3.50 g/d1 200 mg/dl M, 13 g/dl/W, 12 g/d1 4.00 mmol/l 95”,, 1200 /mm’ 0.70 mmolil 50 mzzlj24 40 mmol/24 absent
h h
Day 0
Day 25
89 91 83 88 85 78 47 64 59 78 35 47 25 52 44 17
84 87 75 75 72 69 ‘2 73 49 30 25 38 17 26 22 13
a number of patients (from 100) with xi value under threshold. b Abbreviations: BW, body weight; M, men; W, women.
was expressed body weight.
Description
as the daily
number
of kcal per kg of ideal
of phase 1
Phase 1 analysis was performed to define and select the most reliable and contributive independent variables of the index. To achieve this goal, the following steps were taken: a) the nutritional parameters which in the present series had a normal value on day 0 in most patients, or which had mean values significantly different from a diagnostic group to another, were first deleted; b) the independent variables were defined as the 25day deltas of each selected parameter, Ax, = (xIDIS- xi,&; an important objective was to fulfil requirement (b), independence of the index from overnutrition. To achieve this, we determined for each nutritional parameter a threshold value which corresponds to the lowest value of normal (Table 2). The deltas which were retained finally as independent variables were the only variations inside the pathological area (under threshold): any day 0 or 25 value above threshold was assigned = threshold and delta was not calculated when the day 0 and day 25 were both above threshold; c) the final step was a multiple regression analysis using y (over-all estimation of the nutritional change) as dependent variable [14]. The independent variables Ax, which had a low contributory value to y were then deleted. The contributory value of each variable to y was taken as the standard deviation of that variable times the coefficient b, and divided by the sum of such products for the n independent variables.
The dependent variable y for each patient n l-100 was the result of two physicians’ (JC and JPG) over-all evaluation of ‘how the patient’s nutritional status did improve, or worsen, from day 0 to day 25’. This evaluation was made blindly, taking into account the results of both clinical examination and nutritional measurements, and specified three grades: ‘better’, ‘the same’, and ‘worse’. On day 25 compared to day 0, 61 patients were found ‘better’ from the two evaluations, 13 patients were found ‘better’ from one and ‘the same’ from the other, 17 patients ‘the same’ from the two evaluations, two patients ‘the same’ from one and ‘worse’ from the other, and seven patients ‘worse’ from the two evaluations. The respective numerical values assigned to these five descriptions were + 8, + 3,0, - 2, and -7.
Description
of phase 2
The goal of phase 2 was the development of the coefficients of each selected independent variable of the index. The calculations reproduced exactly the final step of phase 1, but with a reduced number of independent variables and a redefined continuous dependent variable y. The limitations of phase 1 analysis resulted from that the individual parametric data were known when assessing y, that y could only take five arbitrary numerical values, and there was some interobserver disagreement. Particularly, we noticed that some patients with a slight nutritional improvement were very difficult to classify between ‘the same’ and ‘better’. The y value of patients n” 101-150 was then
28
DEVELOPMENT
OF AN INDEX TO ASSESS THE EFFICACY
OF NUTRITIONAL
determined in the following way: on day 0 and day 25, a clinical examination was performed by a physician unaware of the patient’s diagnosis, treatment, and nutritional assessment data (JPG for the patients receiving care from JC, and vice-versa). Several items (physical and intellectual activities, fatigability, behavior, facies, skin, hair, mouth and muscle appearance) were scored by using different scales as published elsewhere [15]. By comparing the changes of the items from day O-25, the physician quantified how about the patient’s nutritional status improved (from 0 to + 10) or worsened (from 0 to - 10) during the 25-day interval. Thus y was a continuous variable from - 10 to + 10.
Description
of phase 3
The index resulting from phase 2 computations was validated prospectively using a linear regression model relating the individual values of the index to y collected according to phase 2. In addition, the individual values of the index were calculated retrospectively in patients YZ’I-100. In the three consecutive groups of patients, the mean values of the index in patients with clearly improved (y > + 3), not significantly changed ( - 4 < y < + 4), and worsened (y < - 3) nutritional status, respectively, were calculated. After determining in patients no 101-150 the cut-off values of the index to recognise clearly improved patients from the remaining, and clearly worsened patients from the remaining, respectively, the number of true positive, true negative, false positive, and false negative inside each consecutive group of patients, and inside the whole group, was calculated and respective sensitivity, specificity, positive accuracy, and negative accuracy of the index to assess clinical nutritional improvement, and deterioration, were obtained.
Calcutations
The analysis of the data was done at the CICG of Grenoble (France) using its H Bull DPS 8/70 computer and programs SPAD and BMDP.
RESULTS Phase 1 (Selection
of the independent
variables)
The parameters xl1 (total lymphocyte count), x,~ (alkaline phosphatases and/or transaminases), and xl6 (edema) were normal on day 0 in most cases (Table 2). They were first dropped. The parameters xi2 (serum magnesium), xIp (urinary sodium), and x,~ (urinary potassium) were significantly more frequently sub-
SUPPORT
IN GASTROINTESTINAL
PATIENTS
normal in patients with intestinal disease (groups CMS and IBD) compared to patients from group WID; we thought then that their incorporation into the next calculations would introduce differences between the groups of patients and they were deleted. Multiple regression analysis with ax,, CI,x2, . . . , Lx,,) as independent variables obtained an encouraging result as multiple R was 0.789 with a F ratio of 13.82. variable Ax,,, (delta of body weight However, expressed as a percent of body weight 3 months before) was associated with a negative sign, and variable Ax, (data cholesterol) had a low fractional contributive value, less than 3”,, . These two variables were deleted. As a result of computations performed in patients n’ l-100, the number of independent variables was thus reduced from the initial 16 to eight.
Phase 2 (Derivation
of the index)
Patients n” 101-150 were very similar to patients n l-100 (Table 1) except that Crohn’s disease was a more frequent diagnosis. This was related to a changing therapeutic approach of patients with Crohn’s disease during recent years. The numbers of day 0 and day 25 xi subnormal values did not differ significantly from those of patients n” l-100. Multiple regression analysis with n x,, n x2, . . , A xg as independent variables led to the index indicated in Table 3. Multiple R was 0.935 with a F ratio of 35.64. Each of the raw coefficients was divided by the smallest one (that of x,) to give standardised coefficients. Values were then rounded to the nearest decade as shown in Table 3. The rounded coefficients are the final ones used for calculating the index. Table 4 gives an example of calculation of the index in one individual patient, and Figure 1 illustrates the card used to collect data and to facilitate computation of the index. Figure 2 gives the regression of the individual values of the index in the patients n’ 101-150. Regression slopes in WID, CMS, and IBD patients, were not significantly different.
Phase 3 (Validation
of the index)
Figure 3 gives the regression of the individual values of the index in the patients n” 151-200. The values of the index were highly related to the clinical evaluation (r =0.86, p
CLINICAL
Table
Derivation
3
of the index
Variable
Item
Delta Delta Delta Delta Delta Delta Delta Delta
Body weight (“” of IBW’) Triceps skin fold (mm) Muscle circumference (cm) Creatinine-height index (“,,) Oral intake (kcal.IBW kg *.d *) Serum albumin (g/d]) Serum transferrin Hemoglobin (g/dl)
x, x2 x3 x4 xs x6 x, xg
29
NUTRITION
Raw coefficient
Standard error
0.22243 0.43961 0.35869 0.02955 0.09639 2.86680 0.01173 0.18131
0.06037 0.19539 0.24943 0.00797 0.02249 0.50630 0.00655 0.14645
Standardised coefficient
Rounded coefficient
“,, contribution 20
70 140 120 10 30 1000 ‘t 60
75.3 148.8 121.4 10.0 32.6 970.2 4.0 61.4
10 6 12
14 25 7 5
a IBW, ideal body weight.
Table
Example
4
for calculation
MB, male, 20-year-old,
of the index
Ileocolonic
Crohn’s
disease
169 cm Ideal body weight
65.9 kg Ideal urinary
creatinine
Day 25
Day 0
Delta Observed value xl x1 x1 x4 x, x, x-
XX
Corrected value
The index
day
EODY WEIGHT
(% of
IBw)
FOLD
(n-m)
SKIN
MI D-ARM MUSCLE CIRCUMFERENCE SPONTANEOUS oRAL lNTAKE
‘cm)
ca I . IBW kg-’
CREATININE-HEIGHT
SERUM ALBUMIN
INDEX
(g/l00
49 kg = 74.4”,, 5.2 mm 20.0 cm 8.9 mmol= 70”,, 2850 kcal= 43.2 3.65 g/d1 225 mg/dl 12.6 g/d1
74.4 5.2 20.0 70 30.0 3.50 200 12.6
(mg/lOO
HEMOGLOBIN
ml)
Format
(g/l00
25
xI
un
:
+854 +140 + 228 ~ 30 + 672 + 580 ‘, 24
meanwiirr-7)
t 346
delta
wI x
70
11.2 14.8
I I I
x
140
male female
22.8 20.9
I I 1
x
120
.day-’
(I,
30.0
I 1I I
x
30
90.0
I I I
x
10
3.50
ml)
for hand calculation
day
0
200 male female
13.0 12.0
1 I 1I I III I III 1
of the index. The value of the index is mean w,
w,
+ 12.2 x 70 +1.0x140 + 1.9 X 120 -3x10 +22.4x 30 +0.58x 1000 not calculated -0.4 x 60
male female
ml)
SERUM TRANSFERRIN
Fig. 1
90.0
xI
x
Corrected value
-
THRESl-UJLD VALUE
TRICEPS
Observed value
62.2 4.2 18.1 73 7.6 2.92 200 13.0
41 kg=62.2”,, 4.2 mm 18.1 cm 9.4 mm01 = 73”,, 500 kcal= 7.6 2.92 g/d1 212 mg/dl 13.2 g/d1
Body weight Triceps skin fold Muscle circumference Urinary creatinine Oral intake Serum albumin Serum transferrin Hemoglobin
12.80 mmolj24
x
1000
X
4
x
60
l-7-n-l
h.
30
DEVELOPMENT
OF AN INDEX TO ASSESS THE EFFICACY
.4 clinical
OF NUTRITIONAL
SUPPORT
IN GASTROINTESTINAL
PATIENTS
-8 assessment
clinical
t
assessment
0
1
Fig. 2 Relation of the index to physician’s appraisal of the over-all nutritional change in patients n 101-150 (Phase 2, development of the index). Squares: WID patients; triangles: CMS patients; circles: IBD patients. and a specificity of 81 O0 for nutritional improvement, and sensitivity and specificity of loo”, for nutritional deterioration. Table 5 gives the statistical results of the index in the three consecutive groups of patients, and in the whole group of 200 patients. The mean values of the index in patients with improved, unchanged, and worsened nutritional status, were not significantly different from one phase to another. The overall accuracy of the index to assess nutritional improvement and deterioration was satisfactory in each phase as in the whole group. 96’,
DISCUSSION This prospective study developed an index which permits objective quantitative assessment of the nutritional response of a 2%day nutritional support in
Fig. 3 Relation of the index to physician’s appraisal of the over-all nutritional change in patients n” 151-200 (Phase 3, validation of the index). Regression slope was Index = 30.43 + 11 (n = 50, r = 0.86, p <: 0.001). Same symbols as Figure 2.
gastro-intestinal patients. The index fulfilled the five requirements we considered important. Furthermore, application of the index in a group of 50 patients who were not used to generate the equation showed that this index was an accurate numerical expression of the overall nutritional change of an individual patient receiving nutritional support. The parameters which were selected from analysis to enter the index were for the most, expected. It is noteworthy that two parameters which are considered universal and basic indicators of nutritional status, body weight and serum-albumin, were found to account for 459: of the index value (Table 3). This high contributive value could be related to the inverse relationship between the deltas of these two parameters when nutritional status did not change clearly in one patient: if body weight increased because of a gain of water, serum-albumin would fall; conversely, dehyd-
CLINICAL
31
NUTRITION
Table 5
Mean f SD, sensitivity, specificity, and positive and negative accuracy of the index to assess nutritional improvement and deterioration.
Patients N l-100 (Phase 1) N 101-150 (Phase 2) N 151-200 (Phase 3) N l-200
Mean * standard deviation improved unchanged worsened +218 f 125 (n=61) +206 f 101 (n=24) +168&69 (n = 24) +204 zr 108 (n= 109)
+48+82 (n=32) +49*70 (n=23) +51 f69 (n=24) +49+ 73 (n=79)
-113f97 (n= 7) -183f45 (n=3) -149 * 12 (n=2) -136i84 (n= 12)
Improved nutritional status? Se Sp PA NA
Worsened nutritional statusb Se Sp PA NA
85
77
85
77
71
97
62
98
87
77
78
87
100
98
75
100
96
81
82
95
100
100
100
100
88
78
83
85
83
98
71
99
n The cut-off value of the index to discriminate improved patients from the remaining was + 100. b The cut-off value of the index to discriminate worsened patients from the remaining was ~ 75. ration could be associated with high serum albumin but would produce a loss of weight; thus an improvement of both body weight and serum-albumin must indicate an improved nutritional status. Likewise, the value of mid-arm muscle circumference is in part negatively related to that of triceps skin fold, and during nutritional recovery, iron deficiency may lead to increased serum transferrin but with decreasing haemoglobin [ 161. Thus, six of the parameters entering the index are linked together in such a way that both improved values indicate necessarily a real improvement. Although it is clear that one nutritional parameter, taken separately, would correlate poorly with tissue repletion [17], this may be not true for a composite index [12]. Finally, a composite index has the capacity to take into account different independent items: the changes of body composition (fat, water, muscle and visceral protein) and the changes in individual capacities of nutritional recovery (caloric intake). However, one may notice that the index does not take into account the patient’s immunological functions, although those are considered as closely related to the nutritional status. The lymphocyte count was normal in most patients before the nutritional support program and thus could not be used as a valuable marker. Skin testing was not performed in this study because we had thought it was an expensive and time-consuming method, and anergy may be induced by extra-nutritional factors [18, 191. An important requirement of the index as a therapeutic index was to demonstrate exclusively the correction of deficiencies and not any over-correction. To fulfill this requirement, it was necessary to develop a relatively complex index, by deleting any supra-normal values. Such a complexity may be a limitation to further utilisation of the index. However, the use of a format (Figure 1) and experience render simple and fast the computations. Finally, the main usefulness of the index would be to allow the objective comparison of different therapeutic nutritional programs, inside a medical unit, and eventually in pluricentric studies.
REFERENCE
[l] Greenberg G R, Jeejeebhoy K N 1979 Intravenous protein-sparing therapy in patients with gastrointestinal disease. Journal of Parenteral and Enteral Nutrition 3: 427-432 [2] Matuchansky C, Morichau-Bauchant M, Druart F, Tapin J 1981 Cyclic (nocturnal) total parenteral nutrition in hospitalized adult patients with severe digestive diseases. Gastroenterology 81: 433-437 [3] Cosnes J, Tello H, Le Quintrec M et al 1983 L’alimentation enterale continue corrige-t-elle la denutrition des affection digestives? Resultats de l’etude longitudinale de 92 malades consecutifs trait& pendant trois h sept semaines. Gastroenterologie Clinique et Biologique 7: 1003-1009 [4] Morin C L, Roulet M, Roy C C, Weber A 1980 Continuous elemental enteral alimentation in children with Crohn’s disease and growth failure. Gastroenterology 79: 1205-1210 [5] Bistrian B R, Blackburn G L, Sherman M 1975 Therapeutic index of nutritional depletion in hospitalized patients. Surgery Gynecology Obstetrics 141: 512-516 [6] Buzby G P, Mullen J L, Matthews D C, Hobbs C L, Rosato E F 1980 Prognostic nutritional index in gastrointestinal surgery. American Journal of Surgery 139: 160-167 [7] Di Costanzo J, Martin J, Cano N et al 1983 Indice nutritionnel pronostique en chirurgie digestive. Gastroenterologie Clinique et Biologique 7: 851-856 [8] Ryan J A Jr, Taft D A 1981 Preoperative nutritional assessment does not predict morbidity and mortality in abdominal operations. Surgical Forum 31: 96-98 [9] Turner W W, Landreneau R J, Toler G F et al 1982 How accurate is nutritional risk classification? Surgical Forum 33: 107-109 [lo] Woolfson AM J 1983 Artificial nutrition in hospital. British Medical Journal 287: 1004-1006 [ll] Baker P B, Detsky A S, Wesson D E et al 1982 Nutritional assessment. A comparison of clinical judgment and objective measurements. New England Journal of Medicine 306: 969-972 [12] Cooper A, Heird W C 1982 Nutritional assessment of the pediatric patient including the low birth weight infant. American Journal of Clinical Nutrition 35: 1132-l 141 [ 131 Blackbum G L, Bistrian B R, Maint B S, Schlamm H T, Smith M F 1977 Nutritional and metabolic assessment of
32
DEVELOPMENT
OF AN INDEX
TO ASSESS
THE
EFFICACY
the hospitalized patient. Journal of Parenteral and Enteral Nutrition 1: 1 l-23 [ 141 Gunst R F, Mason R L 1980 Regression analysis and its applications, Marcel Dekker INC, New York [ 151 Cosnes J, Baumer P, Tello H et al 1987 Aide a la decision d’assistance nutritionnelle au tours des affections digestives chroniques. Gastroentirologie Clinique et Biologique 11: 201-205 [ 161 Delpeuch F, Cornu A, Chevalier P 1980 The effect of iron deficiency anemia on two indices of nutritional status, prealbumin and transferrin. British Journal of Nutrition 43: 385-379 Submission dare: 14 January
1986. Accepted: 18 June 1987
OF NUTRITIONAL
SUPPORT
IN GASTROINTESTINAL
PATIENTS
[ 171 Jeejeebhoy K N, Baker J P, Wolman S L et al 1982 Critical evaluation of the role of clinical assessment and body composition studies in patients with malnutrition and after total parenteral nutrition. American Journal of Clinical Nutrition 35: 1117-l 127 [ 181 McLaughlin G A, Wu A V, Saporoschetz I et al 1979 Correlation between anergy and a circulating immunosuppressive factor following major surgical trauma. Annals of Surgery 190: 297-304 [ 191 Meakins J L, Christou N U, Shizgal H M, McLean L D 1979 Therapeutic approaches to anergy in surgical patients. Annals of Surgery 190: 286296