Appl. Radiat. lsot. Vol.49, No. 5/6, pp. 615-617, 1998 © 1998ElsevierScienceLtd. All rights reserved Printed in Great Britain PII: S0969-8043(97)00085-7 0969-8043/98 $19.00+ 0.00
Pergamon
Monitoring of Fluid Changes in Hospitalized, Malnourished, Guatemalan Children Using Bioelectrical Impedance Spectroscopy (BIS) C H R I S T I A N E P I T H A N 1, M A N O L O M A Z A R I E G O S 2, N O E L W. SOLOMONS 2 and PETER F O R S T t ~The Department of Biological Chemistry and Nutrition, Hohenheim University, Garbenstrasse 30, 70599, Stuttgart, Germany and -'Center for Studies of Sensory Impairment, Aging and Metabolism (CeSSIAM), Diagonal 21, 19-19 zona 11, Guatemala City 01011, Guatemala
Introduction In Guatemala as in many other developing countries, various forms of protein-energy malnutrition (PEM) still prevail. According to the clinical picture, extreme malnutrition has been divided into three types: marasmus, edematous and a mixture of both (McLaren, 1966). Marasmus is characterized by severe wasting of both muscle and subcutaneous fat, marked stunting and no subcutaneous tissue (Suskind et al., 1990). In terms of body composition the major effects are an extreme reduction of the fat mass (FM) and fat-free mass (FFM). Kwashiorkor (also called 'edematous PEM') is a clinical syndrome characterized by fatty liver and visceral enlargement, dermal changes and generalized edema. In this type of malnutrition the major compositional changes relate to the volume of total body water, the degree of hydration of fat-free mass, and the partition of water into intracellular and extracellular spaces (Vettorazi et al., 1990). Finally, the mixed type of PEM which combines features of both, severe tissue wasting and edema, is termed 'marasmic-kwashiorkor'. Technical equipment that easily and non-invasively measures recovery from malnutrition in a clinical setting, which depicts in the case of PEM a situation in which body compartments will experience rapid fluid shifts in association with recovery, is needed if no other equipment is available. Multifrequency spectroscopy could be such a tool. However, due to the small size, irritability and poor cooperation in very young children, there has been a reluctance to take measurements in this population. In the instance of BIS, there is some potential. B1S could be used to monitor shifts between the extra- and intraeellular compartments, but BIS is restricted by the conventional whole-body approach, and questions arise over its use in segmental measurements as a substitute for the conventional whole-body approach. Therefore, the purpose of this study was to evaluate whether BIS
is able to pick up water changes due to diuresis related to recovery from PEM and whether these changes are best reflected in the conventional whole-body approach or in segmental measurements.
Methods and Subjects Population
The study group was composed of 22 children, who were admitted to the General Hospital 'San Juan de Dios' in Guatemala City for acute and severe malnutrition. The age of the groups ranged from 5 to 72 month and the weights from 3.2 to 12.3 kg. Seven children were classified with kwashiorkor by the McLaren classification schemes (McLaren, 1966), seven children were classified with marasmatic-kwashiorkor and eight with pure marasmus. For comparison purposes, a group of 20 children fully recovered from acute malnutrition was recruited from a nutrition unit. Their age and weight profiles matched with those of the study group. They were assessed for weight, height and BIS on one occasion only to determine the profile in terms of BIS indices. Procedures
The children were measured lying supine, with their legs and arms stretched and separated, covered in cotton blankets, wearing only diapers. They were monitored over a period of time from 5 days to several weeks, during their recovery in the hospital. Weight and BIS indices were measured on admission and during the treatment period every second day. BIS measurements were made using a Xitron 4000B analyzer (Xitron Technologies, CA), at the wholebody level by methods reported extensively in the literature and segmental measurements of the arm, trunk, leg and armless-body as described [Mazariegos, 1996 (companion paper)] at frequencies
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Christiane Pithan et al. Table 1. Initial and final comparison for BIS-variable REcw (ohms) for all body segments
Segment
x ± SD initial measurement
Children with kwashiorkor Whole 533 ± body Shoulder-leg 238 ± Arm 330 ± Leg 182 ± Trunk-±psi 64 ± Trunk 43 ± medial
x ± SD final measurement
t-test*
Magnitude of changes'l"
Changes (%)
Changes (%)++ corrected by length
140.5
798 ± 110.8
**
245.2
44.3
33.3
96.9 60.4 79.4 16.8 10.8
413 ± 400 ± 344 ± 67 ± 52 ±
** tt ** ns tt
175.2 69.5 161.4 3.9 8.5
73.6 21.1 88.6 21.6 19.7
52.3 17.6 55.2 6.2 15.9
748 ± 129.04
tt
140.0
20.6
11.9
380 ___82.65 387 ± 70.5 311 ___71.69 68 ± 17.2 47 ± 15.23
ns ns "tt ** ns
98.0 33.0 100.0 18.0 2.0
34.7 9.3 47.4 36.0 4.1
27.6 15.4 28.2 24.4 16.6
797 ± 103.1
ns
18.0
2.3
5.0
414 ± 397 ± 365 ± 70 ± 46 ±
ns ns ns ** ns
31.0 7.3 56.0 -9.0 -7.0
8.1 1.8 18.0 12.0 13.0
1.6 25.0 0.1 18.1 19.1
70.6 51.8 61.8 17.2 10.6
Children with marasmic-kwashiorkor
Whole 608 ± 116.4 body Shoulde~leg 282 ± 75.8 Arm 354 ± 64.2 Leg 211 ± 71.7 Trunk-±psi 50 ± 9.9 Trunk 49 ± 11.8 medial Children with marasmus Whole 774 ± 173.1 body Shoulder-leg 383 ___812.9 Arm 390 ± 92.3 Leg 309 ___69.7 Trunk-±psi 79 ___11.5 Trunk 53 ___6.3 medial
46.7 65.22 73.58 4.67 6.5
*Using paired t-test: **p level _< 0.01; ttp level < 0.05: ns. p level >_ 0.05, not significant. tFinal minus first measurement. +The BIS-index was calculated by dividing the resistance by the length (cm:) of the segment.
f r o m 5 k H z to 1 M H z . T h e r e s i s t a n c e (in o h m s ) o f t h e extra- a n d i n t r a c e l l u l a r c o m p a r t m e n t s w a s calculated using the Cole-Cole modeling program of X i t r o n . In o r d e r to o b t a i n g o o d m e a s u r e m e n t s o n t h e y o u n g , sick a n d restless c h i l d r e n , it w a s n e c e s s a r y to w r a p t h e m in a b l a n k e t , l e a v i n g e x p o s e d t h e specific s e g m e n t to be a s s e s s e d . D a t a analysis M e a n c o m p a r i s o n s were d o n e b e t w e e n t h e initial a n d t h e final m e a s u r e m e n t s (at d i s c h a r g e o r w h e n t h e child w a s c o n s i d e r e d recovered, w h i c h u s u a l l y o c c u r r e d a r o u n d 3 w e e k s a f t e r a d m i s s i o n ) , by u s i n g a p a i r e d t-test. C o r r e l a t i o n coefficients were c a l c u l a t e d b e t w e e n t h e different s e g m e n t s in o r d e r to see t h e i r c o r r e s p o n d e n c e . M e a n c o m p a r i s o n s o f BIS p a r a m e t e r s b e t w e e n t h e c o n t r o l a n d s t u d y g r o u p were carried out using the Duncan New Multiple Range test. F o r all c a s e s t h e significant p v a l u e w a s a d j u s t e d by t h e B o n f e r r o n i c o r r e c t i o n ( M c G u i g a n , 1990).
i n c r e a s e is e x p r e s s e d as a p e r c e n t a g e o f t h e b a s e l i n e values. T h e g r e a t e s t c h a n g e s were s e e n at t h e level o f w h o l e - b o d y , leg a n d a r m l e s s - b o d y , a n d t h e m i n i m u m c h a n g e w a s seen at t h e level o f t r u n k . F o r o n e selected i n d i v i d u a l case t h e c h a n g e s in REcw as m o n i t o r e d o v e r several w e e k s a r e s h o w n in Fig. 1. T h e r e s e e m s to be a different p a t t e r n b e t w e e n t h o s e c h i l d r e n w h o were suffering w i t h k w a s h i o r k o r , marasmatic-kwashiorkor and marasmus, with the m o s t m a r k e d c h a n g e s in t h e k w a s h i o r k o r g r o u p c o m p a r e d to t h e m a r a s m u s g r o u p . F o r t h e Ricw n o p a t t e r n t h a t w a s in a g r e e m e n t w i t h clinical t h e o r y c o u l d be d i s c o v e r e d . F o r REcw all s e g m e n t s a c r o s s t h e t h r e e t y p e s o f m a l n u t r i t i o n c o r r e l a t e d h i g h l y with e a c h o t h e r (r = 0.82 0.96, p < 0.001), w h e r e a s for R,cw t h e c o r r e s p o n d e n c e o f t h e different s e g m e n t s w a s very low (r = 0.1 0.5) w i t h n o s i g n i f i c a n t c o r r e l a t i o n .
V~
700
•
I~
-
sho-l~g~I ./,X
600 I Results
T a b l e 1 s h o w s t h e c o m p a r i s o n s b e t w e e n t h e initial a n d final r e s i s t a n c e o f t h e e x t r a c e l l u l a r s p a c e (REcw) u s i n g b o t h w h o l e - b o d y a n d s e g m e n t a l a p p r o a c h e s for t h e s t u d y g r o u p . T h e r e w a s a n overall i n c r e a s e in REcw a s s o c i a t e d with recovery. W h e n RECW w a s a d j u s t e d by t h e l e n g t h (cm2)/RECW (BIS index-REcw), a clear t r e n d t o w a r d s g r e a t e r c h a n g e s in t h e kwashiorkor and marasmatic-kwashiorkor group with r e s p e c t to t h e m a r a s m u s g r o u p is seen. T h e m e a n
500
0
P
I
I
~
I
I
I
I
I
2
3
4
5 6 7 rneas~ement s
I
8
9
10
II
Fig. 1. Changes in REcw a c r o s s segments in one selected case. The child was followed over 3 weeks during recovery from kwashiorkor.
BIS to measure fluid changes in malnourished children ).05
io0o 900 800 71/11 6o0
41/11 31/11 2011 10t) 0 control
KW
MKW
MA
Fig. 2. Changes in REcw(ohms) of the whole body in the three malnourished groups. Mean comparisons of REcw between initial (dark bars) and final measurements (blank bars). KW = kwashiorkor; MKW = marasmatic-kwashiorkor; MA = marasmus.
Figure 2 shows the level of adjustment between the three groups of malnourished children and the comparison group at admission and discharge from the hospital for the whole-body and the variable RECw. A level of adjustment for the R~cwcould not be detected. Discussion
Nutritional recovery is a relatively slow but steady process, with dramatic changes in body composition. The first phase in the edematous malnutrition is usually characterized by weight reduction, which reflects the loss of the excessive extracellular fluid. The second phase then shows a gain of fluid as the body starts to build new tissues (principally body cell mass). The magnitude and direction of changes of REcw were according to what we expected. Loss of excess fluid for diuresis (in edematous malnutrition) induced a pattern towards an increase in REcw. In other words, the decrease in extracellular water associated with an improvement in the protein status in the child was associated with a significant trend towards an increase in REcw. This suggests that BIS was capable of detecting actual fluid shifts in ECW associated with nutritional recovery. It was interesting to see that the magnitude and direction of the changes tended towards the reference values of the control group. Although the groups were very different and started from different points, they tended towards normality. This study urges further studies to overcome the limitations of the remaining BIS parameters which,
617
according to our preliminary analysis, are very unstable and uninterpretable. Factors such as small size of the conductor (wasted body segments), fluid imbalances, poor compliance in young children and limited capabilities of the current instrumentation are probably responsible for the poor performance in obtaining reliable and accurate R~cw indices. However, as our particular interest resides in the extracellular space, with the current capabilities we can non-invasively monitor fluid shifts in patients with disturbed fluid balance. To describe changes in extracellular resistance as a reflection of extracellular fluid associated with the recovery from malnutrition, BIS proved its ability to produce stable and usable data even in small children with hydration and abnormal fat status, as in PEM. Data for the intracellular space are only partially in agreement with clinical theory for children with PEM. Rtcw does not appear to be a very reliable indicator for intracellular fluid shift at this point of development. Given that some of the segmental measurements such as armless-body and leg were comparable to the whole-body approach, or even reflected greater changes, their use in young and acutely malnourished children can make the usage of this technique easier. Acknowledgements--We would like to thank the authorities and the medical staff of the Nutrition Unit of the Pediatric Department at The General Hospital 'San Juan de Dios' in Guatemala City for their support. We are grateful for the instrumental support of Jim Mathie from Xitron Technologies, Inc. for facilitating the BIS-4000B instrument and providing the disposable electrodes used in the present study. References
McGuigan, F. J. (1990) Experimental psychology. In Methods of Research, 5th edn, pp. 139-146. Prentice Hall, Englewood Cliffs, NJ. McLaren, D. S. (1966) A fresh look at protein-energy malnutrition. Lancet 2, 485-488. Suskind, D., Murthy, K. K. and Suskind, R. M. 0990) The malnourished child. Nestle Nutrition Workshop Series, Vol. 19, Nestle Ltd. Vevey/Raven Press, New York. Vettorazi, C., Molina, S., Grazioso, C., Mazariegos, M., Siu, M. L. and Solomons, N. W. (1990) Bioetectrical impedance indices in protein-energy malnourished children as an indicator of total body water status. In In Vivo Body Composition Studies, Recent Advances, eds S. Yasumura, J. E. Harrison, K. G. McNeill, A. D. Woodhead and F. A. Dilmanian, pp. 45-49. Plenum Press, New York.