Patterns of Catch-Up Growth

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1 Patterns of Catch-Up Growth Caroline C. de Wit, MD 1, Theo C. J. Sas, MD, PhD 2,3, Jan M. Wit, MD, PhD 4, and Wayne S. Cutfield, MD, PhD 1 From embryogenesis to young adulthood, growth rate declines dramatically. This deceleration in growth velocity is most extreme in infancy with a more subtle slowing in growth velocity through mid-childhood, interrupted by the pubertal growth spurt, after which the growth rate gradually declines to zero. 1 While in the first years of life the length of healthy infants can cross the percentiles toward their genetic target height (TH) SDS, height tends to remain within a narrow channel on the growth charts between 3 years and the onset of puberty, close to the same percentile or SDS position. The tendency to keep to this narrow and predictable track of growth is called canalization. 2 An SDS change of >0.25/year is rarely seen in longitudinal growth studies on normal children. 3 A large variety of growth-retarding illnesses, including hypothyroidism, celiac disease (CD), malnutrition, Cushing syndrome or chronic steroid treatment, and growth hormone (GH) deficiency, can lead to a slowing in growth with a downward deviation from the standard growth curve. After release from these growth-inhibiting conditions, exaggerated acceleration in linear growth can occur. In 1963, Prader et al 4 and Tanner 5 introduced the term catch-up growth to describe this period of rapid linear growth in children that followed a period of growth inhibition, leading toward their original growth channel. The term catch-up growth is also used for the growth acceleration seen in 85% of infants born small for gestational age (SGA), 6 although in these cases there is usually no information about the foregoing downward deviation. The term catch-up growth is mostly used for height. Catch-up growth has been defined as a height velocity above the statistical limits of normality for age or maturity during a defined period of time, following a transient period of growth inhibition; the effect of catch-up growth is to take the child towards his/her pre-retardation growth curve. 7 Even though this definition would imply that for a proper assessment of catch-up growth the full growth trajectory has to be evaluated (up to adult height), only few studies on catch-up growth have included all parts of this trajectory (the phases of growth inhibition, growth acceleration, growth maintenance, and puberty and the achieved adult height in comparison with the genetic growth potential). Furthermore, several alternative definitions of catch-up growth have been used, for example (in children born SGA) reaching an SDS of > 2 for the reference population 8 or a cut-off of a change CD GH SGA TH Celiac disease Growth hormone Small for gestational age Target height of >0.67 SDS in the first year. 9 Data on the growth curve after the initial phase of catch-up growth and on the adult height corrected for mid-parental height (TH) are often lacking, presumably because of the difficulties in obtaining frequent growth data over long periods of time. In only a few studies, for example in GH deficiency, 10,11 hypothyroidism, 12,13 and CD, 14 have data on the complete pattern of catch-up growth including data on adult height been described. Catch-up growth also occurs for other growth parameters, such as body weight, body composition, head circumference, and body segments (sitting height and leg length). For example, catch-up growth observed in the early stages after treatment of CD is generally characterized by an initial weight increase before height catches up, thus an initial rise of body mass index. 14 A mismatch between catch-up growth in height and in abdominal fat is seen in babies born preterm or SGA, in which there is greater increase in adiposity than height, which has been associated with a higher risk of cardiovascular disease. 15 Parameters of Catch-Up Growth We have previously argued 16 that the first year height velocity is not suitable as the sole parameter for catch-up growth, because it is highly variable, lacks precision, and incompletely depicts catch-up growth. 17 In addition, the average height velocity for age is highly dependent on the height percentile of the child. For example, if height is to stay on 3rd percentile, a height velocity at approximately the 25th percentile is needed. 16 Furthermore, from a series of height velocities one cannot get a good impression of the position of the patient s height versus the population s reference charts. A better parameter of catch-up growth, particularly when assessed over the full trajectory, is height SDS and its change over time. 16 There is no agreed cut-off criterion for catch-up growth, and we suggest that a sustained increase in height SDS toward the height SDS before the start of growth retardation would suffice as definition. One would expect that the size and speed of the height SDS change during the first years of catch-up growth depend on the distance between height SDS and TH SDS, as well as on age. In fact, this has been observed for GH deficiency. 18 From the 1 The Liggins Institute, University of Auckland, Auckland, New Zealand; 2 Department of Pediatrics, Albert Schweitzer Hospital, Dordrecht, The Netherlands; 3 Department of Pediatrics, Erasmus Medical Centre, Rotterdam, The Netherlands; and 4 Department of Pediatrics, Leiden University Medical Center, Leiden, The Netherlands The authors declare no conflicts of interest /$ - see front matter. Copyright ª 2013 Mosby Inc. All rights reserved

2 THE JOURNAL OF PEDIATRICS Vol. 162, No. 2 Potential Mechanisms of Catch-Up Growth We have previously discussed the 2 main hypotheses that have been proposed to explain catch-up growth: the neuroendocrine hypothesis and the growth plate hypothesis. 7 The neuroendocrine hypothesis was proposed by Tanner in 1963 and is based on the classical endocrine concept of central steering of processes. 5 Tanner suggested that a mechanism possibly located in the hypothalamus is able to compare the size of the body with the individual s expected size for that age. This was called a time tally. If a mismatch is recognized, the body is encouraged to continue growing at a faster-than-normal rate. When the mismatch becomes less distinct, the growth velocity will decrease. 5 So far, no experimental evidence for this hypothesis has been collected. The growth plate hypothesis is based on an old concept proposed by Osborne and Mendel in 1914, who showed that prolonged nutritional deprivation in the rat was followed by growth at an age well beyond the normal growth period of the species. They suggested that age is not the limiting factor for growth but that growth is limited by the intrinsic capacity for growth of the tissue itself. 19 After further work in this area by Williams, 20 a study in rabbits by Baron et al 21 gave this hypothesis its present shape by suggesting that the mechanism for catch-up growth is intrinsic to the growth plate. They proposed that catch-up growth arises from a delay in normal growth plate senescence. During normal growth plate senescence, the proliferative rate of the growth plate chondrocytes diminishes with each successive stem cell cycle. Thus, growth plate senescence is not a function of time per se but rather a function of the cumulative number of divisions the stem cells have undergone. After cessation of suppression of proliferation, in Baron et al s experiments by glucocorticoids or hypothyroidism, the cumulative number of stem cell divisions is lower than expected. After the suppression of proliferation, the cells therefore begin to proliferate at a faster rate than the nonexposed cells, leading to local catch-up growth. 21 None of the 2 hypotheses gives a fully satisfactory explanation for the mechanism of catch-up growth in humans. The neuroendocrine hypothesis lacks experimental support, and the growth plate hypothesis can only explain one specific type of catch-up growth. 22 Published Patterns of Catch-Up Growth In 2 seminal articles, 23,24 Tanner distinguished 3 different growth patterns that potentially lead to the same (normal) adult height. In the first pattern (A), the cessation of the growth restriction is followed by an increased height velocity (up to 4 times the mean velocity for chronologic age), which fully eliminates the growth deficit. When the original growth curve is achieved, height velocity returns to normal. In the second pattern (B), the growth-restricted child grows slightly faster than normal for age but at a normal velocity for bone age, resulting in a longer growth period and a normal adult height. The third pattern (C) shows a growth velocity at the average level for chronologic age but with delayed bone maturation, resulting in growth that goes on for longer than usual. As noted by Tanner and by ourselves, type C formally cannot be considered catch-up growth, because by definition velocity should be above normal for age, 16,24 and we do not discuss this further. Type A catch-up growth is seen as the classic example of catch-up growth and has been reported for several children, such as in some of the cases in the first reports of Prader et al 4 and Tanner. 25 This pattern can be seen in some infants and young children after growth restriction due to CD when a gluten-free diet is introduced, 14 in the majority of young children with hypothyroidism after treatment with levothyroxine, 13 and in many children with GH deficiency who are receiving GH treatment. Children with CD show on average a type B catch-up growth, with a height velocity that is consistent with height age and bone age, 22 conforming to the hypothesis of delayed senescence. 21,26 Another example of type B catch-up growth was given in a report on 2 men with hypopituitarism, in whom GH treatment was started at age 22.7 and 24.3 years at a bone age of years. At ages 27.9 and 29.1 years, respectively, they had gained 22 and 21 cm in height, and their growth velocity was normal for their bone age. 27 An Intermediate Type of Catch-Up Growth (Type AB) We noticed that some catch-up growth curves of children with CD, 14,22,28 hypothyroidism, 13,29 GH deficiency, 11 and preterm born children 30,31 showed a catch-up growth pattern inconsistent with the classic types described by Tanner. Instead, they showed an increased growth velocity in the first years of treatment, followed by a stabilization of height SDS about half of the initial height SDS and genetic TH for a number of years, and a delayed pubertal growth spurt, after which they finally reached an adult height that was close to TH (or lower). If this pattern was arbitrarily defined as a failure to catch up toward the target range (TH 1 SD) within 3 years and further growth toward adult height of >1 SD, it was observed in 4 of 11 children (aged years) with primary hypothyroidism and 2 of 8 children with GH deficiency (aged years) (J.W., unpublished analysis of data reported by Ranke et al 13 and Sas et al 11 ). For illustrative purposes, we show the growth curve of a boy with GH deficiency, who participated in a dose-response study, 11 in comparison with the theoretical curves for type A and B catch-up growth (Figure 1). This type of catch-up growth is intermediate between types A and B. We suggest calling this form catch-up growth type AB, which is characterized by an initial faster growth than normal for bone age, which then passes into a phase of stable height SDS, which remains below TH SDS, until the delayed puberty causes an increase of height SDS toward TH SDS. It is unclear why in some children catch-up growth is abrogated halfway and in others it continues until TH SDS is reached. We speculate that if the underlying disease remains active (eg, inadequately treated CD), treatment is 416 de Wit et al

3 February 2013 COMMENTARY Figure 1. Growth curve of a boy with GH deficiency, treated with GH, compared with the A and B types of catch-up growth according to Tanner (interrupted lines). The boy grew at 2 SDS in the first 2 years, followed by a downward deviation to 4.1 SDS. At 6.6 years, GH treatment was started (0.7 mg/m 2 body surface area/d, at 1 m 2 equivalent to 25 mg/kg body weight/d) and, in the first years of treatment, height SDS gradually increased to 2.4, followed by a stabilization at that height SDS until 17 years of age. Although the onset of puberty (13.2 years) was still within the normal range, the tempo of puberty was slow, and adult height was 173 cm ( 1.5 SDS), close to TH ( 1.3 SDS). 32 nonphysiologic or inadequately dosed (eg, suboptimal dose or poor adherence to GH treatment in children with GH deficiency) or chondrocyte maturation has been adversely affected (by previous exposure to corticoids or sex steroids), type AB may be more likely to occur. In some cases, type AB may also be a manifestation of underlying constitutional delay of growth and puberty or of superimposed illness. Phases of Growth of Children with Catch-Up Growth Ideally, for each child with an acquired growth disorder who shows catch-up growth, information on his or her growth curve should be available for the whole trajectory. In a complete dataset, various phases of growth can be distinguished: (1) the period of normal growth before the onset of the disease (initial growth); (2) poor growth during the disease (growth retardation); (3) the rapid phase of growth acceleration; (4) the maintenance phase; (5) growth in adolescence; and (6) adult height. To assess whether catch-up growth is complete in an individual child, one can follow 2 approaches. First, adult height can be compared with the preillness growth curve, and catchup growth can be considered complete if adult height SDS is close to the original height SDS. Second, adult height can be compared with TH, and at an individual level catch-up growth can be considered complete if adult height is within a range of TH or ,16 At a group level, complete catch-up growth is defined by a mean adult height not statistically different from mean TH. The multiphase approach would imply that there is not one single marker of catch-up but rather a pattern composed of several elements. In the following paragraphs, we discuss what is known about these phases in different conditions where catch-up growth has been described. Phases of Catch-Up Growth in Several Disorders Hypothyroidism In theory, hypothyroidism is the best human model for catch-up growth because it is free of growth constraints associated with chronic disease. However, acquired primary hypothyroidism, usually due to Hashimoto thyroiditis, occurs mainly in older children and adolescents, so that catch-up growth is often concurring with the pubertal growth spurt. The growth retardation observed in hypothyroidism appears to be a direct effect of thyroxine deficiency on skeletal growth, but a secondary reduction of GH secretion and circulating insulin-like growth factor-1 may also play a role. 33 Once thyroxine replacement therapy is commenced, a period of catch-up growth starts. In most young children, Patterns of Catch-Up Growth 417

4 THE JOURNAL OF PEDIATRICS Vol. 162, No. 2 type A catch-up growth is observed, but some children show a growth pattern more consistent with type AB. 13 Because of the unavailability of data on bone age at start of treatment, we cannot rigorously exclude type B catch-up growth in these children. However, growth in the first year is so rapid in some children that it is likely greater than expected for bone age. Even after a prolonged period of growth retardation, a very high growth velocity can be observed. 29 In older children and adolescents, catch-up growth coincides with pubertal development, which is probably the main reason that on average catch-up growth is not complete. 12,29,34 There are very few data on catch-up growth after a long period of thyroxine deficiency in infants born with congenital hypothyroidism, because these children are usually detected very early through congenital hypothyroidism screening. We reported on a 14-year-old patient who had been hypothyroid from birth 29 and showed an extremely fast catch-up growth for 5 years, but in this patient pubertal development occurred at the same time and is presumably responsible for the short adult height. In such cases, administration of a gonadotropin-releasing hormone analog in early puberty may improve adult height outcome. 35,36 CD In affluent countries, CD is one of the most prevalent causes of reversible growth retardation. 37 The pathophysiology of growth retardation in CD has not been fully elucidated. It is generally assumed that nutritional deficiency due to gastrointestinal malabsorption and inflammation plays a major role, but cytokines from the diseased gastrointestinal tract may also be involved. In a retrospective study on the effect of a gluten-free diet, we found several patients who showed a clear type A pattern of catch-up growth and average height SDS increased to 0 SDS, suggestive of complete catch-up growth. 14 However, in a later prospective study we showed that in the first years the average catch-up growth is concordant with type B. 22,28 It is unclear whether a suboptimal catch-up growth is primarily seen in patients who are less adherent to the gluten-free diet. In the first 6-12 months after initiation of the gluten-free diet, weight increases to the predicted weight percentile, followed by an increase of length or height SDS. 14 Besides CD, there are several other conditions that cause undernutrition and subsequent growth inhibition. Often, malnutrition is accompanied by other factors influencing growth including suboptimal hygiene, vitamin deficiency, and unfavorable psychosocial conditions, so that it is difficult to assess catch-up growth. In a rare case of malnutrition in an adolescent with intestinal protein loss secondary to constrictive pericarditis, surgical treatment led to resolution of the protein loss and impressive catch-up growth, resulting in a normal adult height. 16 GH Deficiency The growth of children with GH deficiency can be greatly improved by GH replacement therapy, but in this condition there is no certainty that physiologic conditions have been fully restored. Studies on the growth response of children with GH deficiency have shown that the pattern and completeness of catch-up growth depend on the dose chosen and several other predictive variables. 38 Of 8 children younger than 10 years on a relatively low GH dosage of 0.7 mg/m 2 / d (equivalent to 25 mg/kg/d) 4 showed type A catch-up growth. Two of the remaining children showed type AB catch-up growth resulting in an adult height close to TH (Figure 1), and 2 showed a partial catch-up growth and an adult height below the target range. For the 7 children aged 1-10 years, we calculated mean (SD) height SDS for chronologic age in the first 4 years of GH treatment, as well as height SDS for adjusted age based on initial bone age. The significant positive slope in the first 2 years indicates that the average pattern of catch-up growth is not consistent with type B (Figure 2). On the double dose, all children showed type A catch-up growth (J.W. and T.S., unpublished analysis of data from Sas et al 11 ). It should be noted that even if adult height is in the population range, and close to TH, this can be the result of relatively long legs and a short trunk, a consequence of delayed spontaneous or induced puberty. These abnormal body proportions have been documented several times and have recently been illustrated by the growth curves of identical twins, one of whom had panhypopituitarism. 39 In a review of several studies, 40 as well as in a study of a large database, adult height SDS of children with GH A Height SDS for CA B Height SDS for adjusted age Years of GH treatment Years of GH treatment Figure 2. Height SDS for A, chronological age (CA) and B, adjusted for initial bone age after institution of GH therapy (0.7 mg/m 2 body surface/d) in 7 children with GH deficiency aged 1-10 years. Height SDS for adjusted age significantly increased in the first year (P <.001) and second year (P =.014). In the third and fourth years, no further increase was observed (P =.401 and.618, respectively). Data derived from Sas et al de Wit et al

5 February 2013 COMMENTARY deficiency who were treated with GH was substantially lower than the population mean. 41 It is likely that this is mainly caused by suboptimal GH doses because the Swedish cohort in this study (using a GH regimen of 0.23 mg/kg/wk) reached an adult height close to TH. 10 An additional reason for incomplete catch-up growth may be noncompliance, which appears more frequent that previously expected. 42 Cushing Syndrome In an initial report on catch-up growth by Prader et al 4 and a later article on the follow-up of several patients 43 by Prader, the authors described a girl who had an adrenal tumor resulting in Cushing syndrome. After surgical removal of the tumor, an impressive, although incomplete, type A catch-up growth was observed. 43 A report on 10 children with Cushing disease showed an increase in height velocity shortly after treatment, but adult height was 1.3 SDS. 44 It appears likely that catch-up growth is incomplete because of a combination of factors, such as irreversible effects on growth plates, 7 adrenal androgen excess (and hence estrogen excess), and, subsequently, after pituitary surgery, hypopituitarism. As far as we know, there are no reports on catch-up growth after discontinuation of exogenous glucocorticoid administration. SGA and Prematurity SGA is the common proxy parameter of intrauterine growth restriction. There are multiple known causes of SGA, but in many cases its cause remains unknown. It is well documented that 80%-85% of children born with SGA increase their height SDS above the lower limit of normal in the first year of life, 6,45-48 whereas the remaining children stay below the 3rd percentile. The usual pattern of children born SGA who catch up is that they show increased growth velocity in the first 2-3 years, followed by a stable height SDS in childhood (usually somewhat lower than TH SDS), a normal age at onset of puberty, and an adult height below TH. 6,45-47 There are insufficient data to determine if the pattern of catch-up growth is type B or AB, but catch-up growth is usually incomplete. Similarly to term infants born SGA, most preterm born infants show catch-up growth in weight and length and head circumference after initial postnatal growth failure. 31,48-51 If catch-up growth occurs, it generally starts early in the first months of life and is often achieved within the first years of life. 31,48,49 In a representative study, catch-up growth in height before the age of 3 years occurred in 81% of extremely low birth weight infants, and catch-up growth in weight and head circumference was found in 79% and 81%, respectively. This resulted in an overall achieved catch-up growth for all 3 parameters in 65%. 48 However, late catch-up growth of preterm subjects, by many investigators also labeled as positive percentile crossing, has been described throughout childhood 50 and even in adolescence Various studies show that on average catch-up growth was not complete. Like children born SGA, there are no data to determine the type of catch-up growth. In a cohort of preterm and/or very low birth weight infants followed until young adulthood, 15 the average adult height SDS was 0.55 and 0.60 for males and females, respectively, but body mass index SDS was 0.10 and 0.17 and waist circumference SDS was for males and for females, indicating that catch-up growth did not run in parallel for different measurements and may contribute to a less favorable cardiovascular disease risk profile. 15 Discussion After the cessation or appropriate treatment of a postnatal insult or illness leading to slow growth, catch-up growth is expected. Besides the classic type A catch-up growth and the slower type B, we suggest the existence of an intermediate-type AB characterized by an initial period of fast growth followed by a stable height SDS below TH SDS. Although type catch-up growth is seen in most children treated for primary hypothyroidism and classic GH deficiency and type B in CD and possibly infants born SGA, we observed type AB in some children with primary hypothyroidism, as well as children with GH deficiency who are treated with relatively low doses of GH. We suggest that, in reports on catch-up growth, all phases of the growth curve up to adult height should be described in the context of parental heights. n The authors thank Dr S.M.P.F de Muinck Keizer-Schrama (Erasmus MC, Rotterdam, The Netherlands) for allowing us to use the data on the cases with GH deficiency. Submitted for publication May 30, 2012; last revision received Sep 6, 2012; accepted Oct 4, Reprint requests: Jan M. Wit, MD, PhD, Department of Pediatrics, J6S, Leiden University Medical Center, PO Box 9600, 2300 RC Leiden, The Netherlands. j.m.wit@lumc.nl References 1. Tanner JM, Whitehouse RH, Takaishi M. 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