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Evidence of growth retardation in neonates of apparently normal weight
European Journal of Obstetrics & Gynecology and Reproductive Biology, 45 (1992) 59-62
59
0 1992 Elsevier Science Publishers B.V. All rights resewed 002%2243/92/$05.00 EUROBS 01348
Evidence of growth retardation in neonates of apparently normal weight T. Chard
‘, K. Costeloe
b and A. Leaf
b
Departments of a Obstetrics, Gynaecology and Reproductive Physiology and ’ Neonatal Medicine, St Bartholomew S Hospital Medical College, London, UK
Accepted for publication 2 January 1992
Summary
The aim of this study was to examine the relationship of ponderal index (PI) and the ratio of mid-arm circumference to occipito-frontal circumference (MAC/OFC) to the delivered weight of the child. Measurements were made on 160 singleton neonates with birthweight greater than 2500 g and delivery at 37 weeks or more. Surprisingly, there was a highly significant correlation between PI and birthweight and MAC/OFC and birthweight. We conclude that: (1) values of PI must be evaluated in relation to birthweight, and not against a single absolute standard for the whole normal population; (2) measurement of PI and MAC/OFC may reveal a group of growth-retarded infants amongst infants of apparently ‘normal’ birthweight; and (3) this group of infants might be a target for the extra care normally accorded to the low birthweight infant. Birthweight; Fetal growth retardation; Ponderal index
Introduction
The small-for-gestational-age (SGA) fetus is commonly defined on the basis of a delivered weight below some arbitrary cutoff point within the population range for neonates at that stage of gestation [1,2]. Typically this cutoff point is the tenth or the fifth centile of the normal range. However, this a priori specification has no welldefined logical basis and has two important draw-
Correspondence:
T. Chard, Department of Obstetrics and Gynaecology and Reproductive Physiology, St. Bartholomew’s Hospital Medical College, London EClA 7BE, UK.
backs. The first, and most familiar, is that a proportion of SGA babies must be normal babies whose ‘appropriate’ weight happens to fall at the lower end of a statistical distribution. The second, less obvious drawback is that there must be a significant number of neonates of apparently ‘normal’ weight who are in reality born substantially short of their genetic growth potential. This is the 3500 g fetus which, as the result of placental insufficiency, weighs only 3000 g at birth - a figure which does not place it in an obvious diagnostic category. As an approach to the first of these problems various procedures have been described which might distinguish the small but normal fetus from
60
the fetus which is genuinely growth-retarded. These procedures include measurement of fetal dimensions such as the ponderal index (PI) and the ratio of mid-arm circumference to occipitofrontal circumference (MAC/OF0 The PI is a measure of the relationship between birthweight and body length: the starved child, with a low weight relative to length, will have a low PI and a high risk of perinatal asphyxia [3,4]. Implicit in this definition is that in the normal child all parts of the fetus should grow ‘in parallel’ and there should therefore be no relation between weight and PI. Thus, there is no obvious reason why the body symmetry of a normal 3800 g neonate should differ from that of a normal 3200 g neonate. Similarly, the ratio MAC/OFC is a measure of the relationship between the size of the head and the size of other parts of the body. In the starved child the head would be relatively spared and there would be a decrease in MAC/OFC; in the normal child, as with PI, there is no obvious reason for MAC/OFC to vary with body-weight. The second problem - that of the growth-retarded fetus with an apparently normal body weight - is more difficult to attack. However, if the assumptions about PI and MAC/OFC are correct as set out above, and if there are growthretarded neonates in the normal weight population, then there should be a correlation of birth weight with either or both of PI and MAC/OFC in neonates of apparently normal birthweight. The aim of the present study was to determine whether measurement of PI and MAC/OFC revealed any such relationship.
MAC/OFC
1
2
3
4
5
Quintiles of birthweight Fig. 1. The mean MAC/OFC ratios (+SEM) of neonates of different birthweight (divided into 5 quintiles: 2500-2925 g; 2926-3175 g; 3176-3455 g; 3456-3725 g; 3726-4700 g). The interrupted line is the mean ratio for the whole population.
in g; interquartile range: 3000-3668 g>. Calculations were made of ponderal index (PI) = (BW in g X lOO/(CHL in cmj3 [3] and the ratio MAC/OFC. The relationship of various indices was examined by linear least squares correlation. 2500-4700
Results Subjects and Methods A group of 160 babies was examined within 24 hours of birth at the Homerton Hospital, London E8. All were from singleton pregnancies and the only exclusions were those weighing less than 2500 g and those born at less than 37 weeks gestation. Measurements were made of birthweight (BW), crown-heel length (CHL), mid-arm circumference (MAC), and occipito-frontal circumference (OFC) as described previously 151. The median delivered weight was 3305 g (range:
For the group as a whole, there was a highly significant linear correlation between PI and birthweight (I = 0.56; P < 0.001) and MAC/OFC and birthweight (r = 0.539; P < 0.001). This is clearly illustrated by a comparison of mean PI and MAC/OFC for infants in different birthweight groups (Figs. 1 and 2). The relationship of PI and MAC/OFC to birthweight applied to neonates of both sexes, from primiparae and multiparae, and from mothers of different ethnic groups (Table I). The length of the child was also correlated to PI (r = 0.52; P < 0.041, MAC/OFC
61
2.7
2.6
PI 2.5
2.4 I
1
I
I
I
1
2
3
4
5
Quintiles of birthweight Fig. 2. The mean PI (+SEM) of neonates of different birthweight. The interrupted line is the mean PI for the whole population.
(r = 0.39; P < O.OOl), and birthweight
(r = 0.77;
P < 0.001).
Discussion In a symmetrically grown neonate it would be anticipated that weight and other dimensions would vary in parallel, subject only to random between-subject variation. Thus the large neonate would be expected to show commensurate high values of dimensions such as overall length, and head and arm circumference. If this expectation is true then the ratio of weight to these dimensions, or between one dimension and another,
should be effectively identical for all normal infants. This assumption was implicit in the classic growth charts published by Lubchenco and colleagues [6] which show a normal range for PI in relation to gestation at delivery but without any indication of relation to birthweight. Further: more, Lubchenco and colleagues [6] specifically pointed to the PI as a ratio in which the geometric law of dimensionality is maintained, i.e., the weight of similar bodies is proportional to the cube of their linear dimensions: if the ratio is found not to be constant, then it can only be due to a change in the form of the body. Unexpectedly, the present study shows highly significant correlations between weight, and the ratios of various fetal dimensions. Throughout the weight range, there appears to be a consistent relationship between weight and ponderal index, and weight and MAC/OFC. The PI is a composite of weight and length: the correlation shows that the larger (but ‘normal’) child has a greater body mass relative to its length than does a smaller child. Similarly, the larger child has an arm which is larger in relation to its head than that of a smaller child. However, this does not agree with common belief on the interpretation of PI and MAC/OFC. In the neonate these indices are often used as a guide to the adequacy or otherwise of the intra-uterine environment.
TABLE I The coefficient of linear correlation (r) between birthweight, and ponderal index (PI) and the ratio of mid-arm circumference to occipito-frontal circumference (MAC/OFC) in various groups. In all but one case the probability of significant correlation was < 0.001. The exception was PI and MAC/OFC in the Indo-Pakistani group (P = 0.6 and 0.07) Group
No. of Women
r value PI
MAC/OFC
All women Male child Female child Primiparae Multiparae Caucasians Negro Indo-Pakistani
160 91 69 28 132 87 39 23
0.56 0.57 0.57 0.5 0.58 0.55 0.57 0.34
0.54 0.43 0.75 0.45 0.56 0.53 0.64 0.39
62
Fetal nutrition depends somewhat on maternal nutrition, and there is a relationship between fetal dimensions and maternal nutrition in neonates of normal birthweight [7]. However, maternal nutrition probably accounts for only a small part of the overall variation in the size of the infant and it seems most unlikely that neonatal weight, PI and MAC/OFC would relate solely to the mother’s diet. There are two possible explanations of this phenomenon, one physiological, the other pathological. The physiological explanation is that in a homogeneous population there is a linear relation between PI, MAC/OFC and birthweight. This hypothesis is based simply on observation, and does not imply any mechanism. The alternative explanation is pathological. It supposes that in any so-called normal population there will be a continuum of ‘nutritional status’. Any weight group will therefore include some newborns at the lower end of this continuum, who for clinical purposes might be considered as ‘growth retarded.’ The continuum of nutritional status would yield the apparent correlation between PI, MAC/OFC and birthweight. The existence of a ‘hidden’ group of growth-retarded fetuses has been proposed by a number of authors [8,91 and specific evidence has been presented that infants of normal weight but low PI have a higher than expected neonatal morbidity [4]. The present findings have practical as well as biological implications. First, the demonstration that there is a continuous linear relationship between fetal indices and birthweight suggests that PI and MAC/OFC values cannot be judged against a single absolute standard. Instead, they must be judged against the standard for a given weight range. For example, a PI of 2.1 would be within the normal range for a 2750 g fetus but outside the normal range for a 2750 g fetus. Second, by setting appropriate action lines of weight, PI and MAC/OFC, it might be possible
to identify a group of growth-retarded neonates of apparently normal weight. Altman and Coles [lo] have also suggested that birthweight and indices of growth retardation should be compared by standard deviation scores (SDS): the SDS is the ratio of the number of standard deviations by which birthweight differs from the population mean to the same figure for PI. The identification of growth retarded neonates is, of course, most unlikely to be absolute, but could yield a subgroup of high-risk neonates who might benefit from the closer observation accorded to the growth-retarded child. References 1 Brar HS, Rutherford SE. Classification of intra-uterine growth retardation. Seminars Perinatol. 1988;12:2-10. 2 Goldenberg RL, Cuttrer RD, Hoffman HJ, et al. Intrauterine growth retardation: standards for diagnosis. Am J Obstet Gynecol. 1989;161:271-277. 3 Hoffman J, Bakketeig LS. Heterogeneity of intrauterine growth retardation and recurrent risks. Seminars Perinatol. 1984;8:15-24. 4 Villar J, de Onis M, Kestler E et al. The differential neonatal morbidity of the interuterine growth retardation syndrome. Am J Obstet Gynecol. 1990;163:1.5-157. 5 Meadows NJ, Till J, Leaf A et al. Screening for intrauterine growth retardation using ratio of mid-arm circumference to occipitofrontal circumference. Br Med J. 1986; 292: 1039- 1040. 6 Lubchenco LO, Hansman C, Boyd E. Intra-uterine growth in length and head circumference as estimated from live births at gestational age for 26-42 weeks. Pediatrics. 1966;37:403-408. 7 Doyle W, Crawford MA, Wynn HA et al. The association between maternal diet and birth dimensions. J Nutrit Med. 1990;1:9-17. 8 Chard T. Normality and abnormality. in: Klopper A, ed. Plasma Hormone Assays in Evaluation of Fetal Wellbeing. Edinburgh: Churchill Livingstone, 1976:1-19. 9 Altman DG, Hytten FE. Intra-uterine growth retardation: Let’s be clear about it. Br J Obstet Gynaecol. 1989; 96:1127-1128. 10 Altman DG, Coles ES. Nomograms for precise determination of birthweight for dates. Br J Obstet. Gynaecol. 1980;87:81-86.
59
0 1992 Elsevier Science Publishers B.V. All rights resewed 002%2243/92/$05.00 EUROBS 01348
Evidence of growth retardation in neonates of apparently normal weight T. Chard
‘, K. Costeloe
b and A. Leaf
b
Departments of a Obstetrics, Gynaecology and Reproductive Physiology and ’ Neonatal Medicine, St Bartholomew S Hospital Medical College, London, UK
Accepted for publication 2 January 1992
Summary
The aim of this study was to examine the relationship of ponderal index (PI) and the ratio of mid-arm circumference to occipito-frontal circumference (MAC/OFC) to the delivered weight of the child. Measurements were made on 160 singleton neonates with birthweight greater than 2500 g and delivery at 37 weeks or more. Surprisingly, there was a highly significant correlation between PI and birthweight and MAC/OFC and birthweight. We conclude that: (1) values of PI must be evaluated in relation to birthweight, and not against a single absolute standard for the whole normal population; (2) measurement of PI and MAC/OFC may reveal a group of growth-retarded infants amongst infants of apparently ‘normal’ birthweight; and (3) this group of infants might be a target for the extra care normally accorded to the low birthweight infant. Birthweight; Fetal growth retardation; Ponderal index
Introduction
The small-for-gestational-age (SGA) fetus is commonly defined on the basis of a delivered weight below some arbitrary cutoff point within the population range for neonates at that stage of gestation [1,2]. Typically this cutoff point is the tenth or the fifth centile of the normal range. However, this a priori specification has no welldefined logical basis and has two important draw-
Correspondence:
T. Chard, Department of Obstetrics and Gynaecology and Reproductive Physiology, St. Bartholomew’s Hospital Medical College, London EClA 7BE, UK.
backs. The first, and most familiar, is that a proportion of SGA babies must be normal babies whose ‘appropriate’ weight happens to fall at the lower end of a statistical distribution. The second, less obvious drawback is that there must be a significant number of neonates of apparently ‘normal’ weight who are in reality born substantially short of their genetic growth potential. This is the 3500 g fetus which, as the result of placental insufficiency, weighs only 3000 g at birth - a figure which does not place it in an obvious diagnostic category. As an approach to the first of these problems various procedures have been described which might distinguish the small but normal fetus from
60
the fetus which is genuinely growth-retarded. These procedures include measurement of fetal dimensions such as the ponderal index (PI) and the ratio of mid-arm circumference to occipitofrontal circumference (MAC/OF0 The PI is a measure of the relationship between birthweight and body length: the starved child, with a low weight relative to length, will have a low PI and a high risk of perinatal asphyxia [3,4]. Implicit in this definition is that in the normal child all parts of the fetus should grow ‘in parallel’ and there should therefore be no relation between weight and PI. Thus, there is no obvious reason why the body symmetry of a normal 3800 g neonate should differ from that of a normal 3200 g neonate. Similarly, the ratio MAC/OFC is a measure of the relationship between the size of the head and the size of other parts of the body. In the starved child the head would be relatively spared and there would be a decrease in MAC/OFC; in the normal child, as with PI, there is no obvious reason for MAC/OFC to vary with body-weight. The second problem - that of the growth-retarded fetus with an apparently normal body weight - is more difficult to attack. However, if the assumptions about PI and MAC/OFC are correct as set out above, and if there are growthretarded neonates in the normal weight population, then there should be a correlation of birth weight with either or both of PI and MAC/OFC in neonates of apparently normal birthweight. The aim of the present study was to determine whether measurement of PI and MAC/OFC revealed any such relationship.
MAC/OFC
1
2
3
4
5
Quintiles of birthweight Fig. 1. The mean MAC/OFC ratios (+SEM) of neonates of different birthweight (divided into 5 quintiles: 2500-2925 g; 2926-3175 g; 3176-3455 g; 3456-3725 g; 3726-4700 g). The interrupted line is the mean ratio for the whole population.
in g; interquartile range: 3000-3668 g>. Calculations were made of ponderal index (PI) = (BW in g X lOO/(CHL in cmj3 [3] and the ratio MAC/OFC. The relationship of various indices was examined by linear least squares correlation. 2500-4700
Results Subjects and Methods A group of 160 babies was examined within 24 hours of birth at the Homerton Hospital, London E8. All were from singleton pregnancies and the only exclusions were those weighing less than 2500 g and those born at less than 37 weeks gestation. Measurements were made of birthweight (BW), crown-heel length (CHL), mid-arm circumference (MAC), and occipito-frontal circumference (OFC) as described previously 151. The median delivered weight was 3305 g (range:
For the group as a whole, there was a highly significant linear correlation between PI and birthweight (I = 0.56; P < 0.001) and MAC/OFC and birthweight (r = 0.539; P < 0.001). This is clearly illustrated by a comparison of mean PI and MAC/OFC for infants in different birthweight groups (Figs. 1 and 2). The relationship of PI and MAC/OFC to birthweight applied to neonates of both sexes, from primiparae and multiparae, and from mothers of different ethnic groups (Table I). The length of the child was also correlated to PI (r = 0.52; P < 0.041, MAC/OFC
61
2.7
2.6
PI 2.5
2.4 I
1
I
I
I
1
2
3
4
5
Quintiles of birthweight Fig. 2. The mean PI (+SEM) of neonates of different birthweight. The interrupted line is the mean PI for the whole population.
(r = 0.39; P < O.OOl), and birthweight
(r = 0.77;
P < 0.001).
Discussion In a symmetrically grown neonate it would be anticipated that weight and other dimensions would vary in parallel, subject only to random between-subject variation. Thus the large neonate would be expected to show commensurate high values of dimensions such as overall length, and head and arm circumference. If this expectation is true then the ratio of weight to these dimensions, or between one dimension and another,
should be effectively identical for all normal infants. This assumption was implicit in the classic growth charts published by Lubchenco and colleagues [6] which show a normal range for PI in relation to gestation at delivery but without any indication of relation to birthweight. Further: more, Lubchenco and colleagues [6] specifically pointed to the PI as a ratio in which the geometric law of dimensionality is maintained, i.e., the weight of similar bodies is proportional to the cube of their linear dimensions: if the ratio is found not to be constant, then it can only be due to a change in the form of the body. Unexpectedly, the present study shows highly significant correlations between weight, and the ratios of various fetal dimensions. Throughout the weight range, there appears to be a consistent relationship between weight and ponderal index, and weight and MAC/OFC. The PI is a composite of weight and length: the correlation shows that the larger (but ‘normal’) child has a greater body mass relative to its length than does a smaller child. Similarly, the larger child has an arm which is larger in relation to its head than that of a smaller child. However, this does not agree with common belief on the interpretation of PI and MAC/OFC. In the neonate these indices are often used as a guide to the adequacy or otherwise of the intra-uterine environment.
TABLE I The coefficient of linear correlation (r) between birthweight, and ponderal index (PI) and the ratio of mid-arm circumference to occipito-frontal circumference (MAC/OFC) in various groups. In all but one case the probability of significant correlation was < 0.001. The exception was PI and MAC/OFC in the Indo-Pakistani group (P = 0.6 and 0.07) Group
No. of Women
r value PI
MAC/OFC
All women Male child Female child Primiparae Multiparae Caucasians Negro Indo-Pakistani
160 91 69 28 132 87 39 23
0.56 0.57 0.57 0.5 0.58 0.55 0.57 0.34
0.54 0.43 0.75 0.45 0.56 0.53 0.64 0.39
62
Fetal nutrition depends somewhat on maternal nutrition, and there is a relationship between fetal dimensions and maternal nutrition in neonates of normal birthweight [7]. However, maternal nutrition probably accounts for only a small part of the overall variation in the size of the infant and it seems most unlikely that neonatal weight, PI and MAC/OFC would relate solely to the mother’s diet. There are two possible explanations of this phenomenon, one physiological, the other pathological. The physiological explanation is that in a homogeneous population there is a linear relation between PI, MAC/OFC and birthweight. This hypothesis is based simply on observation, and does not imply any mechanism. The alternative explanation is pathological. It supposes that in any so-called normal population there will be a continuum of ‘nutritional status’. Any weight group will therefore include some newborns at the lower end of this continuum, who for clinical purposes might be considered as ‘growth retarded.’ The continuum of nutritional status would yield the apparent correlation between PI, MAC/OFC and birthweight. The existence of a ‘hidden’ group of growth-retarded fetuses has been proposed by a number of authors [8,91 and specific evidence has been presented that infants of normal weight but low PI have a higher than expected neonatal morbidity [4]. The present findings have practical as well as biological implications. First, the demonstration that there is a continuous linear relationship between fetal indices and birthweight suggests that PI and MAC/OFC values cannot be judged against a single absolute standard. Instead, they must be judged against the standard for a given weight range. For example, a PI of 2.1 would be within the normal range for a 2750 g fetus but outside the normal range for a 2750 g fetus. Second, by setting appropriate action lines of weight, PI and MAC/OFC, it might be possible
to identify a group of growth-retarded neonates of apparently normal weight. Altman and Coles [lo] have also suggested that birthweight and indices of growth retardation should be compared by standard deviation scores (SDS): the SDS is the ratio of the number of standard deviations by which birthweight differs from the population mean to the same figure for PI. The identification of growth retarded neonates is, of course, most unlikely to be absolute, but could yield a subgroup of high-risk neonates who might benefit from the closer observation accorded to the growth-retarded child. References 1 Brar HS, Rutherford SE. Classification of intra-uterine growth retardation. Seminars Perinatol. 1988;12:2-10. 2 Goldenberg RL, Cuttrer RD, Hoffman HJ, et al. Intrauterine growth retardation: standards for diagnosis. Am J Obstet Gynecol. 1989;161:271-277. 3 Hoffman J, Bakketeig LS. Heterogeneity of intrauterine growth retardation and recurrent risks. Seminars Perinatol. 1984;8:15-24. 4 Villar J, de Onis M, Kestler E et al. The differential neonatal morbidity of the interuterine growth retardation syndrome. Am J Obstet Gynecol. 1990;163:1.5-157. 5 Meadows NJ, Till J, Leaf A et al. Screening for intrauterine growth retardation using ratio of mid-arm circumference to occipitofrontal circumference. Br Med J. 1986; 292: 1039- 1040. 6 Lubchenco LO, Hansman C, Boyd E. Intra-uterine growth in length and head circumference as estimated from live births at gestational age for 26-42 weeks. Pediatrics. 1966;37:403-408. 7 Doyle W, Crawford MA, Wynn HA et al. The association between maternal diet and birth dimensions. J Nutrit Med. 1990;1:9-17. 8 Chard T. Normality and abnormality. in: Klopper A, ed. Plasma Hormone Assays in Evaluation of Fetal Wellbeing. Edinburgh: Churchill Livingstone, 1976:1-19. 9 Altman DG, Hytten FE. Intra-uterine growth retardation: Let’s be clear about it. Br J Obstet Gynaecol. 1989; 96:1127-1128. 10 Altman DG, Coles ES. Nomograms for precise determination of birthweight for dates. Br J Obstet. Gynaecol. 1980;87:81-86.