The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 89, Issue suppl 1

Spinal Growth and Development | February 01, 2007

Maturity Indicators in Spinal Deformity

James O. Sanders, MD

Disclosure: In support of his research for or preparation of this work, the author received, in any one year, outside funding or grants in excess of $10,000 from the Scoliosis Research Society. Neither he nor a member of his immediate family received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the author, or a member of his immediate family, is affiliated or associated.

The Journal of Bone and Joint Surgery, Incorporated

J Bone Joint Surg Am, 2007 Feb 01;89(suppl 1):14-20. doi: 10.2106/JBJS.F.00318

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Scoliosis from all causes, with the sole exception of adult degenerative deformity, is a disorder of growth. Physicians who treat spinal deformities in children and adolescents should have a basic understanding of growth and its relationship to the progression of scoliosis and be capable of making an accurate determination of maturity. The purpose of this review is to describe the relationship of growth to the progression of scoliosis, to delineate the various methods of determining maturity, and to describe reasonable ways of evaluating maturity in clinical practice.

Figures in this Article

The relationship of growth to scoliosis was well described by the pioneers of scoliosis treatment^1-4. However, it was the work of Duval-Beaupere^5,6 that clearly demonstrated the close relationship between increased height and scoliosis progression. Her studies showed that curve progression increases markedly at the time of the adolescent growth spurt in both idiopathic and neuromuscular curves and markedly slows or ceases at the time of completion of growth. This is also true for congenital scoliosis⁷. Because of this tight association between maturity and curve behavior, accurate maturity assessment is crucial for predicting prognosis and determining treatment.

Maturation is multidimensional and includes the development of reproductive and secondary sexual characteristics, changes in muscle and fat mass and distribution, and changes in osseous structure. Because curve progression is closely connected with a rapid increase in spinal height at the time of the growth spurt, it is likely that longitudinal growth is the most important dimension of maturity in scoliosis progression. Because serial height information, which is needed to determine where patients are in their growth spurt, is rarely available at the time of patient evaluation, an understanding of the associations among the various maturity markers can be very helpful clinically.

Normal Puberty

The problem with the conventional categorization of children by age is that, in normal children, there is a wide variation in the timing of growth spurt. In children with similar environments, normal pubertal timing can vary by as much as four years⁸. The spinal deformity in a thirteen-year-old girl who is just starting her growth spurt will behave more like that in a nine-year-old girl at a similar stage of growth than that in a fully mature girl of the same age. In assessing spinal maturity, knowledge of normal growth and physical development is very helpful. Humans have two basic pubertal stages, consisting of adrenarche and gonadarche. A child typically undergoes adrenarche, or maturation of the adrenal cortex, between the ages of six and eight years, with the production of the adrenal androgens dehydroepiandrosterone (DHEA), androstenedione, and DHEA-sulfate (DHEA-S)⁹. This manifests physically as pubarche, the time of initial development of pubic and axillary hair. This early hair is usually fine and light, unlike the coarser and darker hair that occurs later in puberty. While the onset mechanism of adrenal cortical maturation remains unknown, abnormal adrenarche timing does not seem to influence normal puberty^10,11. However, the appearance of pubic and axillary hair forewarns of the growth spurt. The second stage, gonadarche, is the activation of the ovary and testis with a dramatic increase in gonadal steroid production and reproductive capability. In girls, gonadarche is manifested by breast development (thelarche) and the onset of menstruation (menarche). Boys undergo testicular enlargement and virilization. After infancy, during the childhood years prior to puberty, normal hypothalamic pulsatile gonadotropin-releasing hormone (GnRH), which is the same as luteinizing hormone-releasing hormone (LHRH), is actively suppressed by neurotransmitters with some input from environmental factors such as body-fat content^8,12-14. The onset of gonadarche occurs when the brain stops actively blocking the secretion of hypothalamic pulsatile GnRH. Neither the blockade nor its release is fully understood, but ?-aminobutyric acid (GABA), neuropeptide Y (NPY), and leptin all play a role. Recent reviews^11,14,15 have covered this topic in more detail.

Both growth hormone (GH) and the sex steroids, particularly estrogen, are necessary for the normal adolescent growth spurt. This is true of both boys and girls. Estrogen appears to be the critical stimulus of the physis, causing its linear growth spurt^16-21. Lower doses of estrogen, such as the amount present during early puberty, stimulate growth, whereas higher doses, as in later puberty, lead to growth cessation. Once the hypothalamus resumes its pulsatile release of GnRH, which is suppressed between infancy and puberty, estrogen is stimulated from the ovaries in girls and from the testis directly and from peripheral aromatization of testosterone in boys, resulting in initial breast development in girls and rapid foot growth in both boys and girls as the first signs of the adolescent growth spurt. This initial estrogen increase stimulates a further release of growth hormones^18,22-24, although there is some experimental evidence from studies of rhesus monkeys (one of the few animals having an adolescent growth spurt similar to humans) that shows that an increased production of growth hormones can start without an initial increase in sex steroids²⁴. Growth hormone acts both directly and indirectly through production of insulin-like growth factor-1 (IGF-1) to stimulate physeal growth. The growth rate peaks about two years later and then slows to cessation after another two years, with estrogen again appearing to be the primary factor causing physeal closure at the end of skeletal growth in both males and females. Since estrogen is the common cause both of secondary sexual characteristics and the growth spurt in girls, secondary sexual characteristics are tightly connected with the growth spurt. In boys, there is more disassociation between sexual maturity and height velocity than in girls. The secondary sexual characteristics of boys develop earlier in the growth spurt as a result of testosterone, and the height velocity occurs later as a result of estrogen, thus explaining why boys are much more sexually mature at the time of the growth spurt than girls are.

Longitudinal Growth and Curve Progression

Several studies have evaluated the relationship between longitudinal growth and curve progression^1,6,25,26. During the first year after birth, the trunk grows very rapidly, but the rate of growth diminishes during each succeeding year and then remains fairly constant from approximately five years of age until adolescence, with some minor growth spurts interspersed. The rate of longitudinal growth is about 5 cm per year from age five years until the adolescent or preadolescent growth spurt. There is then a sharp increase in growth, known as the adolescent growth spurt, at puberty. The maximum rate of this growth spurt is often double or triple the earlier childhood rate and occurs earlier but to a lesser degree in girls than in boys. The period of rapid growth lasts for three to four years (two years before and one to two years after the peak). The spine gains approximately 10 cm in length between birth and five years of age^25,27, accounting for the often rapid progression of congenital and infantile curves during this time. The spine then gains approximately 5 cm in length between the age of five years and adolescence, at which time it grows at a markedly increased rate during the growth spurt. Most of the growth-spurt acceleration is from the trunk and spine, which gain about 10 cm during this period²⁵, rather than from the lower extremities, which have a more constant rate of growth and a less conspicuous growth spurt.

The maximum growth rate is called the peak height velocity (PHV), and the age at the peak height velocity is called the peak growth age (PGA). Maturity may be measured in time intervals from PGA—for example, PGA + 0.5 yr as six months after PHV, or PGA — 1.0 yr as one year before PHV. Curve magnitude at PGA is highly prognostic for scoliosis progression. In their study of idiopathic scoliosis in girls, Little et al.²⁸ demonstrated that patients with a curve of <30° at the time of PHV had only a 4% chance of the curve progressing to a surgical range, whereas patients with a curve of >30° at the time of PHV had an 83% chance of progressing to a surgical range despite bracing. A second, similar study demonstrated a comparable curve progression in boys²⁹; 100% of the curves that were >30° progressed to a surgical range compared with 14% of the lesser curves. The crankshaft phenomenon of progressive deformity, which results from asymmetric growth following a posterior spine fusion in immature patients with scoliosis, is much more likely to occur in patients who undergo fusion before PGA, whereas it is highly unlikely to occur after PGA³⁰.

While measuring the height velocity at sequential visits is currently the best and certainly the most definitive way to determine the timing of PGA, several practical issues are important. Height has a diurnal variation of up to 1.4 cm³¹, and a single misreported height can make the assessment of PHV difficult³². Short-term growth is not linear; it has periods of rapid activity and periods of little activity³³. Therefore, measuring height-velocity changes over short intervals can lead to strange velocity calculations. Height-velocity calculations should be performed at six-month intervals at the minimum. A particular problem with PHV and PGA is that the information only makes sense retrospectively. It is also uncertain whether the peak or the onset of the growth spurt is more important. Measurement of height should ideally be done at the same time of day for every visit. The height should be measured with the patient gently stretched by applying gentle manual upward pressure on the mastoids while ensuring that the feet remain flat on the floor. Sitting-height measurements have the potential to allow a closer look at spinal growth, but we have found it quite difficult to obtain reliable sitting-height measurements. Other potentially useful growth measurements include foot and hand size, arm span, and the distance between the shoulders or acromions. Children typically have substantial growth of the feet and lower extremities before the pubertal growth spurt^34-36. The biacromial distance shows its largest increase after PHV³⁵. Because experience with these methods is so limited, it is not possible to recommend them currently.

Several studies have looked at peak height velocity and its timing. The mean age is about twelve years in girls and fourteen years in boys, with a standard deviation of one year. This means that normal girls (two standard deviations) experience PHV from ages ten to fourteen years and that normal boys experience PHV from ages twelve to sixteen years, with the period of rapid growth occurring two years before and after the peak. PHV and its timing are under tight genetic control and lesser amounts of environmental control³⁷. The results of most studies have shown that girls have a PHV of about 8 cm per year, with a standard deviation of 1, and that boys have a PHV of about 9 cm per year, with a standard deviation that is slightly larger^26,37-40. Therefore, when the growth of a patient who is being followed approaches these values, it can reasonably be assumed that the patient is near PHV.

Secondary Sexual Characteristics

In addition to the rapid gain in height, the other hallmark of maturation is the development of secondary sexual characteristics. Tanner divided these into various clinically useful stages with regard to development of the breasts and pubic hair in girls and the scrotum and pubic hair in boys^19,21,41. Other secondary characteristics that are potentially useful include sweat gland maturation, menarche, voice change, axillary hair, and coarse facial hair. Aside from menarche, none of these have been sufficiently studied to recommend their use at this time.

The pubertal or Tanner stages are excellent maturity measurements⁴⁰ and are highly, although not exactly, correlated with the growth spurt and PHV^25,42,43. Girls typically reach PHV between stages 2 and 3 for breast development and stages 2 and 3 for pubic hair development, whereas boys reach PHV between stages 3 and 5 for penile and testicular growth. In girls, Tanner stage 1 always appears before the PHV and Tanner stage 4 always appears after the PHV⁴⁴. Rapid breast development tends to coincide with the acceleration of growth⁴⁰. Unfortunately, pubertal stages have only been used by a few authors prognostically, notably the French^25,45,46, who have used combinations of pubertal, skeletal, and Risser staging. Duval-Beaupere⁴⁵ found pubertal staging to have a higher correlation with curve progression than skeletal age did. Most North American orthopaedists are uncomfortable in evaluating the secondary sex characteristics of their patients in the context of a scoliosis evaluation. Unfortunately, a self-assessment by the patient is unlikely to provide accurate information^47-49.

Menarche

Menarche is a readily identifiable maturity indicator. Results from a number of studies have indicated that the risk of scoliosis progression is appreciably higher before menarche than after menarche^50-53. Unfortunately, menarche virtually always occurs after PHV^40,43 and is markedly variable compared with the Risser stage (ranging from Risser stage 1 to Risser stage 5)²⁸, and the early menstrual periods are often quite irregular. While menarche is usually a reliable sign that growth velocity is decreasing, it is much too variable to be used for accurate assessments.

Skeletal Maturity

Skeletal age is based on the concept that bones grow and physes mature in an orderly sequence. It is useful to consider skeletal age as a developmental stage rather than a linear "age." The radiographic appearance of any skeletal region is dependent on both the overall hormonal maturational state and the inherent genetic control of each local physis. Any skeletal region with consistent physeal markers is amenable to a determination of skeletal age. Just as active linear growth is dependent on estrogen, the physeal appearances are highly dependent on estrogen levels in both boys and girls. It is a common misperception that growth remains while physes are open; actually, a physis can be nongrowing, particularly toward the end of growth, despite an open appearance on radiographs⁵⁴. The most commonly used markers in patients with scoliosis are the iliac apophysis, the hand, and the wrist; other potential markers include the pelvis, various regions of the spine, the knee, and the elbow. Skeletal ages have been determined by correlating radiographs of children with their ages. Because this method compares groups of children rather than individuals, the accelerations and decelerations are smoothed. At least with hand-bone ages, the process is actually nonlinear, with maturity of the hand bone having its own acceleration and deceleration^22,54-57. Thus, a skeletal age of twelve years and six months is not necessarily six months from a skeletal age of thirteen years but is often closer than that. Skeletal age determinations are based on the examination of normal children. Therefore, the skeletal age may not accurately reflect maturity in a child with medical or developmental issues as it does in normal children^54,58. There is a fairly wide distribution of skeletal age compared with pubertal stages⁴⁰, although the variation is less than with chronological age. While Dimeglio and Bonnel suggested that a skeletal age of thirteen years corresponds to PHV in both boys and girls²⁵, other investigators indicated that PHV occurs at eleven to 11.5 years of age in girls^40,43. We recently reported the relationship of a number of maturity markers relative to scoliosis curve behavior and have found skeletal maturity to be very helpful. These findings are discussed later in this paper⁴⁹.

The Risser sign, which is commonly used as a maturity indicator in scoliosis, is based on the radiographic excursion of iliac apophyseal ossification^3,59,60. The iliac apophysis typically starts ossifying at the anterior superior iliac spine and then extends posteriorly toward the posterior superior iliac spine. Originally used by Risser to denote the completion of spinal growth by fusion of the apophysis to the ilium, the Risser sign has been modified to distinguish levels of maturity by dividing the pelvis into four quarters on the anteroposterior radiographic view. Risser stage 1 designates ossification of the anterior lateral quarter; Risser stage 2, the anterolateral half; Risser stage 3, the anterior three-quarters; Risser stage 4, complete ossification; and Risser stage 5, fusion to the ilium. The advantages of the Risser sign include its ready appearance on standard anteroposterior radiographs of the spine and the fact that it typically proceeds in an orderly fashion. However, because of concerns regarding breast irradiation, most scoliosis radiographs are now made in a posteroanterior rather than an anteroposterior projection. Unfortunately, because of radiographic parallax, the iliac apophyses are much less visible on posteroanterior radiographs. If a lateral radiograph has also been made, the ossification can sometimes be seen more clearly on this view. A further disadvantage of the Risser sign is that it typically appears after the PHV. Risser stage 1 occurs after the growth peak in 85% of patients²⁸. It also does not correlate well with skeletal age and correlates differently in boys and girls. Girls typically have little remaining growth at Risser stage 4, while boys still have substantial growth remaining and may continue to have substantial curve progression between Risser stages 4 and 5⁶¹. We have also seen substantial curve progression in girls between Risser stages 4 and 5⁴⁹.

The utility of the Risser sign can be improved by inclusion of the pelvis, which has a large number of physeal and apophyseal ossification centers, on the radiographs. However, the utility of this method must be balanced against the drawback of increased gonadal irradiation. The triradiate cartilage is currently the most useful site because it typically fuses before initial iliac apophyseal ossification begins and because its fusion also correlates closely with PHV^30,42,62. The Oxford score denotes pelvic bone age and has been used only rarely in the assessment of skeletal maturity in patients with scoliosis. The lesser trochanteric apophysis is rarely visible on routine spine radiographs; therefore, we have used a modification of the Oxford score, ignoring that apophysis. Because many of the pelvic centers are difficult to ascertain, it is helpful to refer to the paper by Acheson⁶³, which describes the times at which the pelvic centers tend to appear. When the Risser sign is not visible, the ischial apophysis will often show a similar progression of ossification and provide additional clues with regard to maturity.

Skeletal Maturity Markers in the Hand and Wrist

Another commonly used skeletal maturity marker in idiopathic scoliosis is a radiograph of the hand, typically referenced to the Greulich and Pyle atlas⁶⁴. The atlas was compiled from radiographs made in the 1930s of primarily white children from Cleveland, Ohio. The atlas assesses both the hand and the wrist on the same film. The Greulich and Pyle atlas has the advantage of being universally available and has reasonable instructions accompanying the figures. However, there are a number of important limitations, the three most important of which are that (1) the hand and wrist do not necessarily mature at the same rate, (2) the atlas does not provide all of the necessary and important details, and (3) unfamiliarity often leads to sloppy usage. There is also substantial user variability, which makes a precise estimation difficult. The Tanner-Whitehouse method attempts to resolve these problems by separating the hand scores from the wrist scores and by assigning skeletal maturity to the individual bones. The digits are a more reliable indicator than the carpus, which adds little to the maturity assessment^65,66. There are several stages in evaluating the digits: at stage one, the epiphysis is not as wide as the metaphysis; at stage two, it is as wide as or wider than the metaphysis; at stage 3, it cups the metaphysis; at stage 4, it begins to fuse; and at stage 5, it is finally fused. We found these stages, particularly the scoring of the metacarpals and phalanges, more closely related to scoliosis progression than were a number of tested maturity markers, including any of the tested hormones, timing of the PHV, Tanner stage, Risser sign, or Oxford staging. The scoring of the metacarpals and phalanges is termed the digital skeletal age (DSA)⁴⁹.The most common error is malpositioning of the hand for the radiograph, with slight flexion of any of the digits making the interpretation difficult. Several investigators are in the process of developing computerized systems to analyze skeletal ages^67-72. While their results are promising, computerized analysis is not part of routine practice. We are currently evaluating a simplified system for clinical use.

Other Skeletal Markers

There are certainly other potential skeletal maturation sites in addition to the hand and the pelvis. The spine itself has a number of markers, particularly ossification of the rib heads and the ring apophysis⁷³. Hoppenfeld et al. compared growth with use of several markers that were visible on routine posteroanterior radiographs⁷³. They found a mean growth of 1.75 cm in the girls and 2.46 cm in the boys between Risser stages 4 and 5 but no growth after Risser stage 5 or after closure of either the rib epiphysis or the proximal humeral growth plates. The ring epiphysis itself is not helpful as it usually remains open until the middle to late twenties⁷⁴. The cervical spine is another potential evaluation site because the vertebrae change shape during the growth spurt^75-78. We have no experience with this method. Similar to the proximal humerus, the elbow is occasionally visible on the posteroanterior radiograph. The time of closure of the distal humeral lateral condyle approximates the time at which a child achieves peak height velocity^25,42 and corresponds with triradiate cartilage closure. While it is conceivable to use these or other markers, their lack of visibility on most routine radiographs limits their utility.

Metabolic Markers of Skeletal Maturity

Rapid skeletal growth is reflected in many metabolic and hormonal markers. Bone remodeling is very rapid, resulting in substantial bone formation and bone resorption products. DHEA and DHEA-S levels rise initially at adrenarche^9,10,22,79, followed by rises in estradiol^17,22,80-82, IGF-1^{18,36,80,83-85}, alkaline phosphatase^82,86-88, and osteocalcin^22,82,88-93. In addition, boys demonstrate large increases in testosterone^22,94,95. The current assessment of these markers is that they are useful if followed serially for increases or decreases but that they are less useful as single values. We assessed several of these factors. IGF-1 showed the best correlation with curve behavior, although not nearly as strong as that seen for skeletal maturation with use of the DSA⁴⁹.

Because calcium plays an active role in platelet aggregation and because platelet aggregation abnormalities have been implicated as a possible factor in the cause of idiopathic scoliosis^96-98, the calcium-binding protein calmodulin has been investigated with regard to its role in idiopathic scoliosis. Kindsfater et al.⁹⁹ examined seventeen adolescent patients who had idiopathic scoliosis, eight patients who had problems that were not related to scoliosis, and two normal volunteers. They found that patients with a progressive scoliosis had a more than sixfold increase in the average level of platelet calmodulin compared with patients with stable curves. While calmodulin may be related to the cause of scoliosis, there is some evidence that it is a mitogen^100,101, meaning that its levels may be related to growth. Thus, whether it is related to the cause of scoliosis or not, it may still be a useful maturity marker.

Recommendations

Obviously, the tight connection between scoliosis and growth provides a strong impetus to find simple and reliable methods to assess maturity. Yet, even as researchers conduct their investigations, clinicians still need practical methods of assessing maturity in their daily practice. We recommend several. First, young, preadolescent patients are reasonably assessed by chronological age. Patients from birth to age three or four years can be assumed to be growing very fast. Children from age five years to the growth spurt can be assumed to be growing slowly, with growth having little impact on scoliosis. Skeletal ages and hormonal assessments are not likely to be helpful during these early stages. As the child approaches eight years of age, adrenarche provides some indication of impending puberty. As children approach the growth spurt, it is helpful to ask questions about the initiation of breast development or about rapid foot growth. Someone who has been trained to assess the stages of secondary sexual characteristics should do so. Patients should not be relied on to accurately assess their own characteristics. The rapid growth spurt occurs while the triradiate cartilages are still open, and these structures should be included on the spine films until they close. If there are concerns about the additional radiation, then a careful assessment of hand skeletal age should be obtained, with a primary reliance on the digits rather than the wrists. Trained personnel should assess the height of the child every six months and should calculate the height velocity. These data provide the best information to determine the time at which the risk of maximum curve progression is greatest and also those times when progression is less likely. It is also helpful for the clinician to be skeptical of his or her ability to assess the Risser sign on posteroanterior radiographs and to not rely on menarche as a reliable maturity marker. If the clinician can assess the Risser sign, then a Risser sign of 4 in girls and a Risser sign of 5 in boys are indicative of very little remaining growth. The Tanner-Whitehouse III skeletal maturity scores, particularly the digital skeletal age and the radiographic appearance of the hand metacarpal and phalangeal epiphyses, correlate very strongly with scoliosis behavior, and we recommend it as a useful addition in maturity assessment of scoliosis patients⁴⁹.

Summary

The timing of the maximum adolescent height velocity is the most important skeletal maturity indicator in patients with scoliosis, regardless of the cause of the scoliosis. Direct measurement of height velocity is prone to error, but a number of other maturity dimensions correlate sufficiently that having a good knowledge of these other dimensions can provide a reasonable assessment of maturity. ?

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Topics

cancer staging ; menarche ; wrist ; puberty ; scoliosis ; spinal deformities

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James O. Sanders; Maturity Indicators in Spinal Deformity. The Journal of Bone & Joint Surgery. 2007 Feb;89(suppl_1):14-20.

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