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Whole body oxygen consumption and anthropometry
CLINICAL NUTRITION (1984) 3:11-16
Whole Body Oxygen Consumption and Anthropometry R. Brown* E. Crrosst, R. A. Little~i, 1"I. B. Stone~ and J. Tresadern$ Department of Surgery (University of Manchester Medical School) and :I:MRC Trauma Unit, Hope Hospital, Eccles Old Road, Salford. Present addresses: * University HoSpital of South Wales, Cardiff. ~"Wythenshawe Hospital, Manchester. S Withington Hospital, Manchester. Reprint requests to PAL
A B S T R A G T Whole body oxygen consumption has been measured and related to several anthropometric indices in 43 control subjects (fed or fasted overnight), in 24 patients who had lost at least 10% body weight during the m o n t h before study and in 16 patients with septic complications following intraabdominal operation who were receiving parenteral nutrition at the time o f the study. T h e r e were good positive correlations between arm muscle circumference and whole body oxygen consumption or resting energy expenditure in all the non-septic groups, although the relationship was changed by a period o f acute weight loss or even an overnight fast. T h e correlations were as good as those obtained with body weight or surface area in both normal and cachectic subjects. It is suggested that the relationship between oxygen consumption and arm muscle circumference may be o f value in determining whether a patient is hypo- or hypermetabolic and may also indicate the m i n i m u m calorie requirements should assistance with feeding be necessary. It is unfortunate that the relationship is very m u c h poorer in the septic patient, where feeding may be a priority, and in s u c h cases the use o f indirect calorimetry is recommended. INTRODUCTION
circumference as the reference base. Krebs [3] has shown experimentally that the differences in the basal rate of heat production in animals of different Size can be attributed mainly to variation in the oxygen consumption of the musculature. Skeletal muscle comprises some 40-45% of body weight, as determined by dissection [4] and the proportions of active tissues to total body weight remains constant during starvation [5]. Voluntary muscle is also not involved in the changes in extracellular fluid volume which occur during nutritional depletion and repletion [6]. Finally it has been shown that arm muscle circumference is a useful indicator of protein stores, especially when assessing differences between groups [7]. Another major diffcuhy arises from the patients' nutritional state. For true basal rates the subject should be in a thermoneutral environment and fasted overnight, unfortunately neither condition can always be achieved clinically. It can be argued [8] that it is of little use studying patients who are fasting if one wants to know more about their metabolism than just the fasting rate of oxygen consumption when fat is the main fuel. Durnin and Passmore [9] have recommended that indirect calorimetry should be done after a light meal without subjecting the patient to the discomfort of a n overnight fast. This possibility has been explored in control subjects and in view of the results it has been used in patients who have suffered serious weight loss. A group of patients with septic complications following operation who were on parenteral nutrition have also been studied. It will be shown that itis possibleto relate wholebody
In recent years there has been an increasing interest in the metabolic effects of surgery and trauma. The application of indirect calorimetry to the study of such patients has made possible the measurement of metabolic rate and the main substrates for oxidation. For ,normal subjects the basal metabolic rate (BMR) is often measured i.e., in a fasting person at rest in a thermo-neutral environment, and expressed in terms ofbody surface area. Several tables have been published showing the expected values of BMR in healthy men and women at different ages [1]. In sick patients one wishes to know whether their metabolic rates are high or low but it is often more difficult to obtain results which are truly basal and can be compared with those given in the tables. One dit2qculty is the choice of reference base for the expression ofresuhs. Age and sex can be determined as can often the height but weight is frequently difficult to measure. Patients and others often have difficulty in estimating weight when it is changing rapidly. Even when weight can be measured its metabolic siguificance may be obscure e.g. if much ofit is interstitial oedema or ascites. A simple reference base is needed and we have explored the possibility that data from indirect calorimetry could be related to arm muscle circumference. The arm was chosen because it is usually readily available and is less likely to be affected by subcutaneous oedema than the leg and there is evidence that the skeletal muscles may behave as a single organ [2]. There are other reasons for the use ofarm muscle 11
12
WHOLE BODY OXYGEN CONSUMPTION AND ANTHROPOMETRY
oxygen consumption to arm muscle circumference in normal subjects and in the weight loss patients provided there is no associated sepsis. A preliminary report of some of the data has been presented [10].
Calorimetry measurements were made when carbohydrate was the only exogenous calorie source and in all cases total calorie intake (carbohydrate plus fat) per day was greater (median 1.6 times, range 1.03-2.32) than the expenditure for that day calculated from the measured metabolic rate. PATIENTS AND METHODS Mid-arm muscle circumference (~MC) was calculated Three groups have been studied: (a) 43 control subjects from mid-arm circumference and triceps skinfold thickness drawn from members of the Unit, friends, hospital staff or (SFT) measured with calipers (Harpenden Skin Fold patients awaiting routine elective surgery (splenectomy 18, Calipers, British Indicators Ltd., St. Albans). All vagotomy and pyloroplasty 2, cholecystectomy 1 and measurements were made by the same person (R.A.L.). Nissen fundoplication 11), none of whom had a history of Height and weight were obtained by standard methods. recent weight loss. (b) 24 patients who had lost at least 10070 Deep body (core) temperature, Tc, was measured with a body weight during the menth before study. All but one of zero-gradient aural thermometer (Addison Process Control the patients in this group had a malignant lesion of the Ltd., Beckenham). Enviromental temperatures were oesophagus and/or stomach. The exception was a case of measured with either a whirting hygrometer or a Light pancreatitis. (c) 16 patients with septic complications 'minilab' (Light Laboratories Ltd., Brighton). The ambient following an intra-abdominal operation. The severity ofthe temperatures were similar for all groups and were as sepsis was assessed by a scoring method described follows:-- dry bulb 20.2-26.8°C (median 23.9°C), wet previously [11] and the sepsis scores ranged from 5-21. bulb 12.2-21.4°C (median 16.5°C). Indirect calorimetry measurements were made with a The metabolic rate or resting energy expenditure [14] Beckman Metabolic Measurement cart (MMC) using the was calculated from oxygen consumption, respiratory Advanced Bedside programme as described in detail exchange ratio and the calorie equivalent of oxygen. previously [12]. Briefly, the patient was conneced to the Oxygen c o n s u m p t i o n (VOz) and resting energy MMC using either a rubber mouth-piece, two-way valve expenditure, both corrected to a core temperature of 37°C, and nose clip or a Royal Air Force face mask (with or have been expressed in terms of body surface area, body without a helmet). The method chosen was largely weight, body weight o.7sand arm muscle circumference. determined by patient comfort although in some of the The correction to a core temperature of 37°C was done to cachectic patients the RAF mask could not be used. The improve the comparison of results from different subjects MMC was always calibrated immediately before use (and and the assumption was made that there is a 10% increase often checked after use) with air and a mixture of 12% 02 (or decrease) in oxygen consumption per rise (or fall) in and 5% CO2 (BOC Special Gases, London -- certificate of core temperature e.g. [15]. It could be argued that mean analysis). The main advantage of the Advanced Bedside body temperature would be a better basis for comparison programme is that gaseous exchange data is only calculated but its calculation using the Burton formula [16] involves when sampling in the 'breath by breath' mode indicates measurements of mean skin temperature. Also it is not that the patient is in a steady state. For example data are not known whether this formula is valid for the very thin accepted if the patient is hyperventilating and the end-tidal cachectic person or for the septic patient. (or alveolar) CO: tension is falling. The validation of the The results were analysed statistically by both parametric A~MC for gas exchange measurements has been described and non-parametric methods [17]. in detail by Damask et al. [13]. All measurements were made after the subjects had been lying supine or propped up in bed for at least 30 rain and RESULTS were continued for at least a further 20 rain whenever possible. However in the very ill septic patients this was Some details of the subjects studied are shown in the Table. not always achieved and data were accepted after 6-8 min The age ranges of the patients in the three groups were [12]. The control subjects (Group A) were studied 2-3 h. similar although the median was considerably higher in after eating a hospital meal of 300-500 Kcal (fed) and of those with acute weight-loss. The controls were selected to these 12 were also studied after an overnight fast (post- cover a wide range of body weights, although the median absorptive). Food hntake in the acute weight-loss patients was higher than in the other groups which included (Group 'B) was reduced due to the severe dysphagia. patients who had lost weight. It is of interest that body However all had received a finely divided hospital meat or weight was still above 90°70 of 'ideal' in 13 of the acute Ca!oreen and~milk (250--400 Kcal) 2,3.5 h . before study. weight'loss patients, n o n e of whom were clinically T h e calorie content Of themeals was determined b y the dehydrated (e.g. blood urea 2.2-8.4 retool/l, median 4.3). hospital diet!clans. AI! t h e septic patients i had central The resting energy expenditures (corrected to a T c of ven0us~catheters and were:receiving: parenteral nutrition. 37°C) were variable and in the: control and weight-loss
CLINICAL NUTRITION
13
Table 1 Details of subjects studied and their resting energy expenditure.
n( )
Group
A.
CONTROL
Body weight (Kg)
Body height (cm)
Surface area (m2)
Median
Median
Median
Median
43(20)
35 (20-:76)
64.0 (43.0-125.0)
165 (147-193)
(1.32-2.5o)
24(14)
63 (20-82)
52.5 (33.3-76.4)
165 (148-185)
1.70 1.28-2.00)
16(9)
45 (23-81)
60.2 (32.0-75.5)
164 (147-180)
(1.21-1.93)
(fed)
S. A C U T E WEIGHT LOSS C. SEPSIS
Age (y)
1.72
1.69
Body weight as % i d e a l (1) Median
expenditure(2)
Restingenergy
103 (80-145) 90* (59-t20)
91.4 ± 2.16"* (70.1-125.8) 79.5 ± 5.03* (37.6-133.0)
97 (62-116)
94.2 + 2.65 69.0-120.4)
as % predicted (3) Mean ± SEM
1. Ideal weights taken from the Metropolitan Life Insurance tables (1959) 2. REE corrected to a core temperature of 37°C. 3. Predictedvalues taken from Fleisch (1). * Significantlydifferent from 100% at p<0.01 (Wilcoxonsigned rank test). ** Significantlydifferent from 100% at p<0,001 (Wilcoxonsigned rank test). groups were significantly lower than the metabolic rates predicted from the Fleisch tables [1] (Table). In the fed control subjects there were significant (p < 0.001, n-- 44) positive correlat.;ons between oxygen consumption corrected to a Tc of 37°C (VO2T) and arm muscle circumference (r=0.7978 Fig. 10, body weight (r=0.7918), body weight oTs (r=0.7905) and surface area (r=0.8051). The correlations were also significant using the Kendall rank Method, showing that assumptions do not have to be made about the distribution of the data. Similar significant (p<0.001, n---44) correlations were fouhd between resting energy expenditure (REE) and the anthropometric measurements, AMC (r--0.7822), body
300
(/02(T) mlmiff' 200
o#o~
100
_ 0.
I ....
i 10
t
! 20
t
t 30
AMC
t ...... J 40 cm
Fig. I Relationship between oxygen consumption (correctedto
a body temperature of 37 oC , V O 2 T ) and arm muscle circumference (AMC) in control fed subjects.Forty four measurements were made in 43 subjectsand each measurement was used as an independent data point; The one subject in whom two measurements were made gained a lot of weight during the study. The regression line shown (y., 37.8 ± 27.9 + (10.1 ± 1,2)x)is the lineof best fitfor all subjectswith its 95% confidence limits.
weight (r=0.7019), body weight o75 (r=0.7039), surface area (r=0.7319). There was no correlation between either VO2T or REE and triceps skin-fold thickness. After an overnight fast oxygen consumption was reduced and the regression line relating VOlT to AMC (r=0.9339) was displaced below the 'fed' line (p<0.02, analysis of covariance) without a change in slope (Fig. 2a). After an" acute non septic weight loss of more than 10% body weight, VOlT was again positively correlated (p<0.001, n=24) with AMC (r=0.8170), body weight (r---0.7564), body weight o.75(r=0.7604) and surface area (r=0.7435) and not correlated with SFT. The slope of the line relating VO2T to AMC in these patients was significantly greater (p< 0.01, analysis of covariance)than in the fed or post-absorptive control subjects (Fig. 2b). A total of 31 measurements were made in 16 septic patients. The measurements were repeated whenever possible as AMC and sepsis score changed during the period of sepsis. If all the measurements were used as independent data points there was no correlation between VO2 or VOlT and any of the anthropometric measurements (P just greater than 0.05 for AMC). However with the inclusion of sepsis score as a third variable the relationship between VOlT (but not VO2) and AMC was significant (p<0.05) although the correlation coefficient was much lower (0.4044) than those in the other groups. If the data from each patient in whom several measurements had been made were averaged (i.e. each patient now contributed only one point to the relationship) there was a significant correlation between VO2T (not VO2) and AMC (p<0.05Kendall rank correlation test or by either the weighted or unweighted least mean squares fit.) The interpretation of the data from these patients is complicated by the fact that eight of them had suffered an acute weight loss comparable to that seenin Group b. In the septic patiems without weight loss VO2T (9 measurements in g)patients)was evenly distributed about the control post-absorptive line. However inthe Septic patients
14
WHOLEBODYOXYGENCONSUMPTIONAND ANTHROPOMETRY
(a)
DISCUSSION
300 ';'%(T) mlmin" 200
100
I 0
_
t
'SO
I
I
20
I
t
.
!
__
30 AMC
I
40 em
(b) aoo '102 (T) mlmin" 200
loo
o
lO
20
30 AMC
,~o
cm
Fig. 2 (a) Relationships between oxygen consumption (correctedto a body temperature of 37°C~VO2T) and arm muscle circumference(AMC) in control fed subjects (as shown in Fig. 1) and in 12 control subjects fasted overnight (hatched). The regressionlines shown are the lines of best fit with their 95% confidencelimits. The regression line in the 'fasted' subjects (y = -94.4 4. 30.7 + (10.2 :t: t.2)x) was displaced below the 'fed' line (p < 0.02, analysis of covariance)without a change in slope. (b) Relationships between oxygen consumption (corrected to a body temperature of 37*C-VOzT) and arm muscle circumference(AMC) in control fed subjects (as shown in Fig. 1) and in acute non-septic weight loss patients (hatched). Twenty four measurements were made in the 24 acute weight loss patients and each measurement was used as an independent data point. The regression line~ shown are the lines of best fit with their 95% Confidencelimits, The slope of the regresson line inthe weight loss patients (y = "221.2 + 56.5 + 07.0 + 2.6)x) was greater (p < 0.01), analysis of covariance)than in the control fed subjects. with weight loss all the VO2T measurements (23 in eight patienis) lay ab0ve the regression line for the acute nonseptic~wetght-!Oss,:~padents (p <0.005: X~:test), !n other wor~::o.xygen c 0 n ~ p d o a w a s highe~than expected even afie~ ~rredtion to a T c of 37°C.
The present results show that there is good positive correlation between arm muscle circumference (AMC) and whole body oxygen consumption or resting energy expenditure and that this relationship is changed by a period of rapid weight loss. The correlation is as good as those obtained with body weight or surface area in both normal and cachectic subjects. The resting metabolic rates measured in the control fed subjects, although agreeing well with other recent studies (18-20), were significantly lower than those predicted from Fleisch. This may be because although Fleisch values are derived from the data of other workers claiming to represent basal metabolic rates (e.g. 2I) they correspond most closely to those calculated by Husby [22] From data For standard metabolic rates (i.e. measured under standard conditions) rather than truly basal values. The difficulty of obtaining such basal values in the clinical environment is, perhaps, emphasised by the definition of the basal metabolism as the minimum rate of energy expenditure compatible with life [23]. The reduced resting energy expenditures in the patients with acute weight loss, which was not due to a lowered body temperature, confirms earlier findings (e.g. five). The finding of a relatively low resting energy expenditure in many of the septic patients has already been discussed [24]. The choice of a reference base for comparisons of metabolic rate has always been controversial. For example, Kleiber (1947) suggested that body weight 0.75 was most useful both for inter- and intraspecies comparisons. However, Heusner (1982) has recently shown that Kleiber's 0.75 mass exponent is a statistical artefact and does not describe the relationship between basal metabolism and body mass. The debate has centered on the assessment of active tissue mass and the conventional use of surface area seems tO be of limited value especially when considering changes in metabolic rate during starvation [27-28]. For example, is the surface area of a subject who has lost weight rapidly that ofthe subject before weight loss or that of a normal subject at the new weight? The use of arm muscle circumference as a reference has already been justified (vide supra) and comparison of the correlations shows that body weight and surface area are no better than arm muscle circumference as a reference base. The effect of prolonged reduced food intake on the relationship between oxygen consumption and AMC is of interest. It is different to an acute Fast (12 h) where ~.Ithough VO~ is reduced the slope of the relationship is unchanged. The increase in slope in :the weight-loss patients suggests that at low arm muscle circumferences the VO2 in these subjects will be less than that of a subject who normally has :a small AMC. Thus the fall. in oxygen consumption during prolonged reduced food intake is not due just tO the iedtlcti6n in mus~ie m~issbut isals0 due ioa reduction in metabolic activily of the rnuscle. A s t h e
CLINICAL NUTRITION
number of cells in skeletal muscle remains constant during an acute weight loss [29] it would seem that the oxygen consumption of the individual cells is decreased as part o f an adaptation to a markedly reduced food consumption. However it must be remembered that as whole body and not just muscle oxygen consumption is being measured the adaptations may not be occurring in muscle at all but elsewhere in the body, for example, in the splanchnic bed
[30]. The data in the septic patients are not easy to interpret but there is a suggestion that in those who have also suffered an acute weight loss oxygen consumption is raised even after correction for pyrexia. In other words the sepsis is of itself increasing metabolic rate, perhaps an abscess is contributing directly to the hypermetabolic state [31]. An alternative explanation might be that infused carbohydrate has a greater calorigenic effect in the depleted compared to the non-depleted septic patient [18,32]. It would therefore seem that in both 'normal' and acute weight loss patients, but not in septic patients, arm muscle circumference can be used as an indicator o f oxygen consumption and hence of e n e r g y expenditure. Arm
REFERENCES [1] Fleisch A 1951 Le metabolisme basal standard et sa determination au moyen du 'Metabocalculator', Helvetica Medica Acta 18:23-27 [2] Moxam J, Morris A J R, Spiro S G a al 1981 Contractile properties and fatigue of the diaphragm in man. Thorax 36:164-168 [3] Krebs H 1950 Body size and tissue respiration. Biochemica Biophysica Acta 4:249-254 [4] Forbes R M, Cooper A R, Mitchell H H 1953 The composition of the adult human body as determined by chemical analysis. Journal of Biological Chemistry 203: 359-366 [5] Keys A, Brozek J, Henschel Aet al 1950 The Biology of Human Starvation. Minneapolis: University of Minnesota Press [6] Starker P M, Askanazi J, Lasala P Aet al 1983 The effect of parenteral nutrition repletion on muscle water and electrolytes. Implications for body composition. Annals of Surgery 198:213-217 [7] Collins J P, McCarthy I D, HiU G L 1979 Assessment of protein nutrition in surgical patients the value of anthropometrics. American Journal of Clinical Nutrition 32:1527-1530 [8] Stoner H B 1982 Assessment of energy expenditure. Proceedings of the Nutrition Society 41:349-353 [9] Durnin J V G A, Passmore R 1967 Energy, work and Leisure. Heinemann, ~London [10] Gross E, Brown R, Little R Aet al 1981 Whole body oxygen consumption and anthropometry. British Journal of Surgery 68: 364, 59A [11] Elebute E A, Stoner H B 1983 The grading of sepsis. British Journal of Surgery 70:29-31 [12] Stoner H B, Little R A, Gross E, Milewsld P 1981 : Metabolic complication s of parenteral nutrition. Acta Chirurgica Beigica 80:125-131
15
muscle circumference, or perhaps one o f the other closely related anthropometric indices such as arm muscle area [33], is at least as useful as body weight. It is also much easier to measure, especially in emergency situations or when the patient is, for example, on traction. It is hoped that the relationship established between oxygen consumption and arm muscle circumference will be o f value in determining whether a patient is hypo- or hypermetabolic at different stages o f the response to accidental trauma and also indicate their minimal calorie requirements should assistance with feeding be indicated. It is unfortunate that this latter consideration does not seem to apply to the septic patient, where feeding may be a priority, and in such cases the use of indirect calorimetry may be indicated.
ACKNOWLEDGEMENTS Our thanks are due to the Consultant Surgical Staff of the Hope Hospital, Salford, or access to the patients under their care. We also wish to thank those who acted as controls, Mrs R. Atkins, Miss P. Bithell and the hospital dieticians for their excellent assistance.
[13] Damask M C, Weissman C, Askanazi Jet al 1982 A systematic method for validation of gas exchange measurements. Anesthesiology 57 3:213-218 [!.!] Elwyn D H, Kinney J M, Gump F E et al 1980 Some metabolic effects of fat infusions in depleted patients. Metabolism 29:125-132 [15] Wilmore D W 1977 The Metabolic Measurement of the Critically Ili. Plenum, New York [16] Burton A C 1946 Clothing and heat exchanges. Federation Proceedings 5:344-351 [17] Snedecor G W, Cochran W G 1967. Statistical Methods, 6th ed. Ames: Iowa State University Press [18] Askanazi J, Carpentier Y A, Elwyn D Het al 1980 Influence of total parenteral nutrition on fuel utilisation in injury and sepsis. Annals of Surgery 191:40-46 [19] Barot L R, Rombeau J L, Feurer I D, Mullen J L 1982 Calorie requirements in patients with inflammatory bowel disease. Annals of Surgery 195:214-218 [20] Quebbeman E J, Ausman R K, Schneider T C 1982 A reevaluation of energy expenditure during parenteral nutrition, Annals of Surgery 195:282-286 [21] Boothby W M, Sandiford I 1922 Summary of the basal metabolism data on 8614 subjects with special reference to the normal standards for the estimation of BMR. Journal of Biological Chemistry 54:783-803 [22] Husby J 1948 Calculation of the basal metabolism. Acta Medica Scandinavica 129:582-592 [23] Mitchell H H 1962 Comparative Nutrition of Men and Domestic Animals. Academic Press, New York [24] Stoner H B, Little R A, Frayn K N e t al 1983 The effect of sepsis on the oxidation of carbohydrate and fat. British Jo~'nal of Surgery 70:32-35 [25] Kleiber M 1947 Body size and metabolic rate. Physiological Reviews 27:511-541 [26] Hensner A A 1982 Energy metabolism and body size. Is the 0.'i5 mass exponent of Kleiber's equation a statistical artefact? Respiratory Physiology 48:1212
16
WHOLEBODYOXYGENCONSUMPTIONAND ANTHROPOMETRY
[27] Benedict F G 1916 The relationship between body surface and heat production especiallyduring prolonged fasting. American Journal of'~hysiology 41:292-308 [281 Taylor H L, Keys A 1950 Adaptation to calorie restriction. Science 112:215-218 [29] Young V R 1970 Skeletal muscle and cardiac muscle and regulation. In: Munro H N (ed) Mammalian Protein Metabolism, Vol. IV, Academic Press. pp 586-674 [30] Grande F, Anderson J T~ Keys A 1958 Changes of basal metabolic rate in man in semistarvationand refeeding. Journal of Applied Physiology 12:230-238 Submission date 24 Nov. 83. Accepted after revision 2 Feb. 8,L
[31] Wilmore D Wj Aulick L H.~ Mason A D, Pruitt B A 1977 Influence of the burn wound on local and systemic responses to injury. Annals of Surgery 186:444-456 [32] Elwyn D H, Gump F E, Munro H Met al 1979 Changes in nitrogen balance of depleted patients with increasing infusions of glucose. American Journal of Clinical Nutrition 32:1597-1611 [33] Heymsfield S B, Mc/vlanus C, Smith Jet al 1982 Anthropometrie measurements of muscle mass: revised equations for calculating bone-free arm muscle area. American Journal of Clinical Nutrition 36:680-690
Whole Body Oxygen Consumption and Anthropometry R. Brown* E. Crrosst, R. A. Little~i, 1"I. B. Stone~ and J. Tresadern$ Department of Surgery (University of Manchester Medical School) and :I:MRC Trauma Unit, Hope Hospital, Eccles Old Road, Salford. Present addresses: * University HoSpital of South Wales, Cardiff. ~"Wythenshawe Hospital, Manchester. S Withington Hospital, Manchester. Reprint requests to PAL
A B S T R A G T Whole body oxygen consumption has been measured and related to several anthropometric indices in 43 control subjects (fed or fasted overnight), in 24 patients who had lost at least 10% body weight during the m o n t h before study and in 16 patients with septic complications following intraabdominal operation who were receiving parenteral nutrition at the time o f the study. T h e r e were good positive correlations between arm muscle circumference and whole body oxygen consumption or resting energy expenditure in all the non-septic groups, although the relationship was changed by a period o f acute weight loss or even an overnight fast. T h e correlations were as good as those obtained with body weight or surface area in both normal and cachectic subjects. It is suggested that the relationship between oxygen consumption and arm muscle circumference may be o f value in determining whether a patient is hypo- or hypermetabolic and may also indicate the m i n i m u m calorie requirements should assistance with feeding be necessary. It is unfortunate that the relationship is very m u c h poorer in the septic patient, where feeding may be a priority, and in s u c h cases the use o f indirect calorimetry is recommended. INTRODUCTION
circumference as the reference base. Krebs [3] has shown experimentally that the differences in the basal rate of heat production in animals of different Size can be attributed mainly to variation in the oxygen consumption of the musculature. Skeletal muscle comprises some 40-45% of body weight, as determined by dissection [4] and the proportions of active tissues to total body weight remains constant during starvation [5]. Voluntary muscle is also not involved in the changes in extracellular fluid volume which occur during nutritional depletion and repletion [6]. Finally it has been shown that arm muscle circumference is a useful indicator of protein stores, especially when assessing differences between groups [7]. Another major diffcuhy arises from the patients' nutritional state. For true basal rates the subject should be in a thermoneutral environment and fasted overnight, unfortunately neither condition can always be achieved clinically. It can be argued [8] that it is of little use studying patients who are fasting if one wants to know more about their metabolism than just the fasting rate of oxygen consumption when fat is the main fuel. Durnin and Passmore [9] have recommended that indirect calorimetry should be done after a light meal without subjecting the patient to the discomfort of a n overnight fast. This possibility has been explored in control subjects and in view of the results it has been used in patients who have suffered serious weight loss. A group of patients with septic complications following operation who were on parenteral nutrition have also been studied. It will be shown that itis possibleto relate wholebody
In recent years there has been an increasing interest in the metabolic effects of surgery and trauma. The application of indirect calorimetry to the study of such patients has made possible the measurement of metabolic rate and the main substrates for oxidation. For ,normal subjects the basal metabolic rate (BMR) is often measured i.e., in a fasting person at rest in a thermo-neutral environment, and expressed in terms ofbody surface area. Several tables have been published showing the expected values of BMR in healthy men and women at different ages [1]. In sick patients one wishes to know whether their metabolic rates are high or low but it is often more difficult to obtain results which are truly basal and can be compared with those given in the tables. One dit2qculty is the choice of reference base for the expression ofresuhs. Age and sex can be determined as can often the height but weight is frequently difficult to measure. Patients and others often have difficulty in estimating weight when it is changing rapidly. Even when weight can be measured its metabolic siguificance may be obscure e.g. if much ofit is interstitial oedema or ascites. A simple reference base is needed and we have explored the possibility that data from indirect calorimetry could be related to arm muscle circumference. The arm was chosen because it is usually readily available and is less likely to be affected by subcutaneous oedema than the leg and there is evidence that the skeletal muscles may behave as a single organ [2]. There are other reasons for the use ofarm muscle 11
12
WHOLE BODY OXYGEN CONSUMPTION AND ANTHROPOMETRY
oxygen consumption to arm muscle circumference in normal subjects and in the weight loss patients provided there is no associated sepsis. A preliminary report of some of the data has been presented [10].
Calorimetry measurements were made when carbohydrate was the only exogenous calorie source and in all cases total calorie intake (carbohydrate plus fat) per day was greater (median 1.6 times, range 1.03-2.32) than the expenditure for that day calculated from the measured metabolic rate. PATIENTS AND METHODS Mid-arm muscle circumference (~MC) was calculated Three groups have been studied: (a) 43 control subjects from mid-arm circumference and triceps skinfold thickness drawn from members of the Unit, friends, hospital staff or (SFT) measured with calipers (Harpenden Skin Fold patients awaiting routine elective surgery (splenectomy 18, Calipers, British Indicators Ltd., St. Albans). All vagotomy and pyloroplasty 2, cholecystectomy 1 and measurements were made by the same person (R.A.L.). Nissen fundoplication 11), none of whom had a history of Height and weight were obtained by standard methods. recent weight loss. (b) 24 patients who had lost at least 10070 Deep body (core) temperature, Tc, was measured with a body weight during the menth before study. All but one of zero-gradient aural thermometer (Addison Process Control the patients in this group had a malignant lesion of the Ltd., Beckenham). Enviromental temperatures were oesophagus and/or stomach. The exception was a case of measured with either a whirting hygrometer or a Light pancreatitis. (c) 16 patients with septic complications 'minilab' (Light Laboratories Ltd., Brighton). The ambient following an intra-abdominal operation. The severity ofthe temperatures were similar for all groups and were as sepsis was assessed by a scoring method described follows:-- dry bulb 20.2-26.8°C (median 23.9°C), wet previously [11] and the sepsis scores ranged from 5-21. bulb 12.2-21.4°C (median 16.5°C). Indirect calorimetry measurements were made with a The metabolic rate or resting energy expenditure [14] Beckman Metabolic Measurement cart (MMC) using the was calculated from oxygen consumption, respiratory Advanced Bedside programme as described in detail exchange ratio and the calorie equivalent of oxygen. previously [12]. Briefly, the patient was conneced to the Oxygen c o n s u m p t i o n (VOz) and resting energy MMC using either a rubber mouth-piece, two-way valve expenditure, both corrected to a core temperature of 37°C, and nose clip or a Royal Air Force face mask (with or have been expressed in terms of body surface area, body without a helmet). The method chosen was largely weight, body weight o.7sand arm muscle circumference. determined by patient comfort although in some of the The correction to a core temperature of 37°C was done to cachectic patients the RAF mask could not be used. The improve the comparison of results from different subjects MMC was always calibrated immediately before use (and and the assumption was made that there is a 10% increase often checked after use) with air and a mixture of 12% 02 (or decrease) in oxygen consumption per rise (or fall) in and 5% CO2 (BOC Special Gases, London -- certificate of core temperature e.g. [15]. It could be argued that mean analysis). The main advantage of the Advanced Bedside body temperature would be a better basis for comparison programme is that gaseous exchange data is only calculated but its calculation using the Burton formula [16] involves when sampling in the 'breath by breath' mode indicates measurements of mean skin temperature. Also it is not that the patient is in a steady state. For example data are not known whether this formula is valid for the very thin accepted if the patient is hyperventilating and the end-tidal cachectic person or for the septic patient. (or alveolar) CO: tension is falling. The validation of the The results were analysed statistically by both parametric A~MC for gas exchange measurements has been described and non-parametric methods [17]. in detail by Damask et al. [13]. All measurements were made after the subjects had been lying supine or propped up in bed for at least 30 rain and RESULTS were continued for at least a further 20 rain whenever possible. However in the very ill septic patients this was Some details of the subjects studied are shown in the Table. not always achieved and data were accepted after 6-8 min The age ranges of the patients in the three groups were [12]. The control subjects (Group A) were studied 2-3 h. similar although the median was considerably higher in after eating a hospital meal of 300-500 Kcal (fed) and of those with acute weight-loss. The controls were selected to these 12 were also studied after an overnight fast (post- cover a wide range of body weights, although the median absorptive). Food hntake in the acute weight-loss patients was higher than in the other groups which included (Group 'B) was reduced due to the severe dysphagia. patients who had lost weight. It is of interest that body However all had received a finely divided hospital meat or weight was still above 90°70 of 'ideal' in 13 of the acute Ca!oreen and~milk (250--400 Kcal) 2,3.5 h . before study. weight'loss patients, n o n e of whom were clinically T h e calorie content Of themeals was determined b y the dehydrated (e.g. blood urea 2.2-8.4 retool/l, median 4.3). hospital diet!clans. AI! t h e septic patients i had central The resting energy expenditures (corrected to a T c of ven0us~catheters and were:receiving: parenteral nutrition. 37°C) were variable and in the: control and weight-loss
CLINICAL NUTRITION
13
Table 1 Details of subjects studied and their resting energy expenditure.
n( )
Group
A.
CONTROL
Body weight (Kg)
Body height (cm)
Surface area (m2)
Median
Median
Median
Median
43(20)
35 (20-:76)
64.0 (43.0-125.0)
165 (147-193)
(1.32-2.5o)
24(14)
63 (20-82)
52.5 (33.3-76.4)
165 (148-185)
1.70 1.28-2.00)
16(9)
45 (23-81)
60.2 (32.0-75.5)
164 (147-180)
(1.21-1.93)
(fed)
S. A C U T E WEIGHT LOSS C. SEPSIS
Age (y)
1.72
1.69
Body weight as % i d e a l (1) Median
expenditure(2)
Restingenergy
103 (80-145) 90* (59-t20)
91.4 ± 2.16"* (70.1-125.8) 79.5 ± 5.03* (37.6-133.0)
97 (62-116)
94.2 + 2.65 69.0-120.4)
as % predicted (3) Mean ± SEM
1. Ideal weights taken from the Metropolitan Life Insurance tables (1959) 2. REE corrected to a core temperature of 37°C. 3. Predictedvalues taken from Fleisch (1). * Significantlydifferent from 100% at p<0.01 (Wilcoxonsigned rank test). ** Significantlydifferent from 100% at p<0,001 (Wilcoxonsigned rank test). groups were significantly lower than the metabolic rates predicted from the Fleisch tables [1] (Table). In the fed control subjects there were significant (p < 0.001, n-- 44) positive correlat.;ons between oxygen consumption corrected to a Tc of 37°C (VO2T) and arm muscle circumference (r=0.7978 Fig. 10, body weight (r=0.7918), body weight oTs (r=0.7905) and surface area (r=0.8051). The correlations were also significant using the Kendall rank Method, showing that assumptions do not have to be made about the distribution of the data. Similar significant (p<0.001, n---44) correlations were fouhd between resting energy expenditure (REE) and the anthropometric measurements, AMC (r--0.7822), body
300
(/02(T) mlmiff' 200
o#o~
100
_ 0.
I ....
i 10
t
! 20
t
t 30
AMC
t ...... J 40 cm
Fig. I Relationship between oxygen consumption (correctedto
a body temperature of 37 oC , V O 2 T ) and arm muscle circumference (AMC) in control fed subjects.Forty four measurements were made in 43 subjectsand each measurement was used as an independent data point; The one subject in whom two measurements were made gained a lot of weight during the study. The regression line shown (y., 37.8 ± 27.9 + (10.1 ± 1,2)x)is the lineof best fitfor all subjectswith its 95% confidence limits.
weight (r=0.7019), body weight o75 (r=0.7039), surface area (r=0.7319). There was no correlation between either VO2T or REE and triceps skin-fold thickness. After an overnight fast oxygen consumption was reduced and the regression line relating VOlT to AMC (r=0.9339) was displaced below the 'fed' line (p<0.02, analysis of covariance) without a change in slope (Fig. 2a). After an" acute non septic weight loss of more than 10% body weight, VOlT was again positively correlated (p<0.001, n=24) with AMC (r=0.8170), body weight (r---0.7564), body weight o.75(r=0.7604) and surface area (r=0.7435) and not correlated with SFT. The slope of the line relating VO2T to AMC in these patients was significantly greater (p< 0.01, analysis of covariance)than in the fed or post-absorptive control subjects (Fig. 2b). A total of 31 measurements were made in 16 septic patients. The measurements were repeated whenever possible as AMC and sepsis score changed during the period of sepsis. If all the measurements were used as independent data points there was no correlation between VO2 or VOlT and any of the anthropometric measurements (P just greater than 0.05 for AMC). However with the inclusion of sepsis score as a third variable the relationship between VOlT (but not VO2) and AMC was significant (p<0.05) although the correlation coefficient was much lower (0.4044) than those in the other groups. If the data from each patient in whom several measurements had been made were averaged (i.e. each patient now contributed only one point to the relationship) there was a significant correlation between VO2T (not VO2) and AMC (p<0.05Kendall rank correlation test or by either the weighted or unweighted least mean squares fit.) The interpretation of the data from these patients is complicated by the fact that eight of them had suffered an acute weight loss comparable to that seenin Group b. In the septic patiems without weight loss VO2T (9 measurements in g)patients)was evenly distributed about the control post-absorptive line. However inthe Septic patients
14
WHOLEBODYOXYGENCONSUMPTIONAND ANTHROPOMETRY
(a)
DISCUSSION
300 ';'%(T) mlmin" 200
100
I 0
_
t
'SO
I
I
20
I
t
.
!
__
30 AMC
I
40 em
(b) aoo '102 (T) mlmin" 200
loo
o
lO
20
30 AMC
,~o
cm
Fig. 2 (a) Relationships between oxygen consumption (correctedto a body temperature of 37°C~VO2T) and arm muscle circumference(AMC) in control fed subjects (as shown in Fig. 1) and in 12 control subjects fasted overnight (hatched). The regressionlines shown are the lines of best fit with their 95% confidencelimits. The regression line in the 'fasted' subjects (y = -94.4 4. 30.7 + (10.2 :t: t.2)x) was displaced below the 'fed' line (p < 0.02, analysis of covariance)without a change in slope. (b) Relationships between oxygen consumption (corrected to a body temperature of 37*C-VOzT) and arm muscle circumference(AMC) in control fed subjects (as shown in Fig. 1) and in acute non-septic weight loss patients (hatched). Twenty four measurements were made in the 24 acute weight loss patients and each measurement was used as an independent data point. The regression line~ shown are the lines of best fit with their 95% Confidencelimits, The slope of the regresson line inthe weight loss patients (y = "221.2 + 56.5 + 07.0 + 2.6)x) was greater (p < 0.01), analysis of covariance)than in the control fed subjects. with weight loss all the VO2T measurements (23 in eight patienis) lay ab0ve the regression line for the acute nonseptic~wetght-!Oss,:~padents (p <0.005: X~:test), !n other wor~::o.xygen c 0 n ~ p d o a w a s highe~than expected even afie~ ~rredtion to a T c of 37°C.
The present results show that there is good positive correlation between arm muscle circumference (AMC) and whole body oxygen consumption or resting energy expenditure and that this relationship is changed by a period of rapid weight loss. The correlation is as good as those obtained with body weight or surface area in both normal and cachectic subjects. The resting metabolic rates measured in the control fed subjects, although agreeing well with other recent studies (18-20), were significantly lower than those predicted from Fleisch. This may be because although Fleisch values are derived from the data of other workers claiming to represent basal metabolic rates (e.g. 2I) they correspond most closely to those calculated by Husby [22] From data For standard metabolic rates (i.e. measured under standard conditions) rather than truly basal values. The difficulty of obtaining such basal values in the clinical environment is, perhaps, emphasised by the definition of the basal metabolism as the minimum rate of energy expenditure compatible with life [23]. The reduced resting energy expenditures in the patients with acute weight loss, which was not due to a lowered body temperature, confirms earlier findings (e.g. five). The finding of a relatively low resting energy expenditure in many of the septic patients has already been discussed [24]. The choice of a reference base for comparisons of metabolic rate has always been controversial. For example, Kleiber (1947) suggested that body weight 0.75 was most useful both for inter- and intraspecies comparisons. However, Heusner (1982) has recently shown that Kleiber's 0.75 mass exponent is a statistical artefact and does not describe the relationship between basal metabolism and body mass. The debate has centered on the assessment of active tissue mass and the conventional use of surface area seems tO be of limited value especially when considering changes in metabolic rate during starvation [27-28]. For example, is the surface area of a subject who has lost weight rapidly that ofthe subject before weight loss or that of a normal subject at the new weight? The use of arm muscle circumference as a reference has already been justified (vide supra) and comparison of the correlations shows that body weight and surface area are no better than arm muscle circumference as a reference base. The effect of prolonged reduced food intake on the relationship between oxygen consumption and AMC is of interest. It is different to an acute Fast (12 h) where ~.Ithough VO~ is reduced the slope of the relationship is unchanged. The increase in slope in :the weight-loss patients suggests that at low arm muscle circumferences the VO2 in these subjects will be less than that of a subject who normally has :a small AMC. Thus the fall. in oxygen consumption during prolonged reduced food intake is not due just tO the iedtlcti6n in mus~ie m~issbut isals0 due ioa reduction in metabolic activily of the rnuscle. A s t h e
CLINICAL NUTRITION
number of cells in skeletal muscle remains constant during an acute weight loss [29] it would seem that the oxygen consumption of the individual cells is decreased as part o f an adaptation to a markedly reduced food consumption. However it must be remembered that as whole body and not just muscle oxygen consumption is being measured the adaptations may not be occurring in muscle at all but elsewhere in the body, for example, in the splanchnic bed
[30]. The data in the septic patients are not easy to interpret but there is a suggestion that in those who have also suffered an acute weight loss oxygen consumption is raised even after correction for pyrexia. In other words the sepsis is of itself increasing metabolic rate, perhaps an abscess is contributing directly to the hypermetabolic state [31]. An alternative explanation might be that infused carbohydrate has a greater calorigenic effect in the depleted compared to the non-depleted septic patient [18,32]. It would therefore seem that in both 'normal' and acute weight loss patients, but not in septic patients, arm muscle circumference can be used as an indicator o f oxygen consumption and hence of e n e r g y expenditure. Arm
REFERENCES [1] Fleisch A 1951 Le metabolisme basal standard et sa determination au moyen du 'Metabocalculator', Helvetica Medica Acta 18:23-27 [2] Moxam J, Morris A J R, Spiro S G a al 1981 Contractile properties and fatigue of the diaphragm in man. Thorax 36:164-168 [3] Krebs H 1950 Body size and tissue respiration. Biochemica Biophysica Acta 4:249-254 [4] Forbes R M, Cooper A R, Mitchell H H 1953 The composition of the adult human body as determined by chemical analysis. Journal of Biological Chemistry 203: 359-366 [5] Keys A, Brozek J, Henschel Aet al 1950 The Biology of Human Starvation. Minneapolis: University of Minnesota Press [6] Starker P M, Askanazi J, Lasala P Aet al 1983 The effect of parenteral nutrition repletion on muscle water and electrolytes. Implications for body composition. Annals of Surgery 198:213-217 [7] Collins J P, McCarthy I D, HiU G L 1979 Assessment of protein nutrition in surgical patients the value of anthropometrics. American Journal of Clinical Nutrition 32:1527-1530 [8] Stoner H B 1982 Assessment of energy expenditure. Proceedings of the Nutrition Society 41:349-353 [9] Durnin J V G A, Passmore R 1967 Energy, work and Leisure. Heinemann, ~London [10] Gross E, Brown R, Little R Aet al 1981 Whole body oxygen consumption and anthropometry. British Journal of Surgery 68: 364, 59A [11] Elebute E A, Stoner H B 1983 The grading of sepsis. British Journal of Surgery 70:29-31 [12] Stoner H B, Little R A, Gross E, Milewsld P 1981 : Metabolic complication s of parenteral nutrition. Acta Chirurgica Beigica 80:125-131
15
muscle circumference, or perhaps one o f the other closely related anthropometric indices such as arm muscle area [33], is at least as useful as body weight. It is also much easier to measure, especially in emergency situations or when the patient is, for example, on traction. It is hoped that the relationship established between oxygen consumption and arm muscle circumference will be o f value in determining whether a patient is hypo- or hypermetabolic at different stages o f the response to accidental trauma and also indicate their minimal calorie requirements should assistance with feeding be indicated. It is unfortunate that this latter consideration does not seem to apply to the septic patient, where feeding may be a priority, and in such cases the use of indirect calorimetry may be indicated.
ACKNOWLEDGEMENTS Our thanks are due to the Consultant Surgical Staff of the Hope Hospital, Salford, or access to the patients under their care. We also wish to thank those who acted as controls, Mrs R. Atkins, Miss P. Bithell and the hospital dieticians for their excellent assistance.
[13] Damask M C, Weissman C, Askanazi Jet al 1982 A systematic method for validation of gas exchange measurements. Anesthesiology 57 3:213-218 [!.!] Elwyn D H, Kinney J M, Gump F E et al 1980 Some metabolic effects of fat infusions in depleted patients. Metabolism 29:125-132 [15] Wilmore D W 1977 The Metabolic Measurement of the Critically Ili. Plenum, New York [16] Burton A C 1946 Clothing and heat exchanges. Federation Proceedings 5:344-351 [17] Snedecor G W, Cochran W G 1967. Statistical Methods, 6th ed. Ames: Iowa State University Press [18] Askanazi J, Carpentier Y A, Elwyn D Het al 1980 Influence of total parenteral nutrition on fuel utilisation in injury and sepsis. Annals of Surgery 191:40-46 [19] Barot L R, Rombeau J L, Feurer I D, Mullen J L 1982 Calorie requirements in patients with inflammatory bowel disease. Annals of Surgery 195:214-218 [20] Quebbeman E J, Ausman R K, Schneider T C 1982 A reevaluation of energy expenditure during parenteral nutrition, Annals of Surgery 195:282-286 [21] Boothby W M, Sandiford I 1922 Summary of the basal metabolism data on 8614 subjects with special reference to the normal standards for the estimation of BMR. Journal of Biological Chemistry 54:783-803 [22] Husby J 1948 Calculation of the basal metabolism. Acta Medica Scandinavica 129:582-592 [23] Mitchell H H 1962 Comparative Nutrition of Men and Domestic Animals. Academic Press, New York [24] Stoner H B, Little R A, Frayn K N e t al 1983 The effect of sepsis on the oxidation of carbohydrate and fat. British Jo~'nal of Surgery 70:32-35 [25] Kleiber M 1947 Body size and metabolic rate. Physiological Reviews 27:511-541 [26] Hensner A A 1982 Energy metabolism and body size. Is the 0.'i5 mass exponent of Kleiber's equation a statistical artefact? Respiratory Physiology 48:1212
16
WHOLEBODYOXYGENCONSUMPTIONAND ANTHROPOMETRY
[27] Benedict F G 1916 The relationship between body surface and heat production especiallyduring prolonged fasting. American Journal of'~hysiology 41:292-308 [281 Taylor H L, Keys A 1950 Adaptation to calorie restriction. Science 112:215-218 [29] Young V R 1970 Skeletal muscle and cardiac muscle and regulation. In: Munro H N (ed) Mammalian Protein Metabolism, Vol. IV, Academic Press. pp 586-674 [30] Grande F, Anderson J T~ Keys A 1958 Changes of basal metabolic rate in man in semistarvationand refeeding. Journal of Applied Physiology 12:230-238 Submission date 24 Nov. 83. Accepted after revision 2 Feb. 8,L
[31] Wilmore D Wj Aulick L H.~ Mason A D, Pruitt B A 1977 Influence of the burn wound on local and systemic responses to injury. Annals of Surgery 186:444-456 [32] Elwyn D H, Gump F E, Munro H Met al 1979 Changes in nitrogen balance of depleted patients with increasing infusions of glucose. American Journal of Clinical Nutrition 32:1597-1611 [33] Heymsfield S B, Mc/vlanus C, Smith Jet al 1982 Anthropometrie measurements of muscle mass: revised equations for calculating bone-free arm muscle area. American Journal of Clinical Nutrition 36:680-690