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The Journal of Clinical Endocrinology & Metabolism Vol. 89, No. 12 6100-6104
Copyright © 2004 by The Endocrine Society

COMMENT

Growth Hormone Therapy in Children after Cranial/Craniospinal Radiation Therapy: Sexually Dimorphic Outcomes

Shulamit E. Lerner, Guo Jun Michael Huang, Donald McMahon, Charles A. Sklar and Sharon E. Oberfield

Division of Pediatric Endocrinology (S.E.L., G.J.M.H., S.E.O.), Children’s Hospital of New York-Presbyterian, New York, New York 10032; Division of Endocrinology (D.M.), New York Presbyterian Hospital, New York, New York 10032; and Division of Pediatric Endocrinology (C.A.S.), Memorial Sloan Kettering Cancer Center, New York, New York 10021

Address all correspondence and requests for reprints to: Dr. Sharon E. Oberfield, Division of Pediatric Endocrinology, Children’s Hospital of New York-Presbyterian, 630 West 168th Street, PH-5E-522, New York, New York 10032. E-mail: seo8{at}columbia.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Radiation therapy (RT) to the craniospinal region in childhood affects final height. The use of GH treatment (GHRx) in children after cranial or craniospinal RT results in variable improvement in final height. Nineteen children (12 males and 7 females) with tumors of the head, treated with cranial or craniospinal RT and subsequently with GHRx, were assessed for final height. Two outcome measures of efficacy of GHRx were used: Y1 = final height SD score (SDS) corrected for genetic potential, using midparental sex-adjusted target height (SATH) SDS, and Y2 = change in height SDS from predicted final height SDS pre-GHRx to actual final height SDS post-GHRx. The median age at diagnosis was 5.4 yr, the median RT to the hypothalamic-pituitary axis was 40 Gy, the median spinal RT dose in 13 of 19 of the subjects treated was 36 Gy, and the median years post-RT to GHRx was 4.8 yr. Adjuvant chemotherapy was used in 12 of 19 patients. All but one (optic glioma) had a lesion anatomically distant from the suprasellar region. The effects of age at diagnosis, sex, L-T4 or GnRH agonist use, conventional vs. hyperfractionated RT, spinal RT, dose of spinal or cranial RT, chemotherapy, peak stimulated GH, dose and duration of GHRx, age at GHRx, time interval between RT and GHRx initiation, bone age, and height SDS at the start of GHRx were also assessed. Y1girls best correlated with younger age at diagnosis and im vs. sc GHRx. Y2girls best correlated with delayed bone age and younger age at diagnosis [Y1girls = –9.95 + 0.38 (age in years at diagnosis) + 3.11[GH method (1 = im; 2 = sc)]; r2 = 0.898; P = 0.02; Y2girls = –3.54 + 1.8 (bone age – age in years) + 0.334 (age at diagnosis in years); r2= 0.956; P = 0.02]. Both Y1boys and Y2boys were strongly associated with spinal RT and younger age at diagnosis or treatment [Y1boys = –11.22 + 4.65 [spinal RT (1 = yes; 2 = no)] + 0.396 (age in years at diagnosis); r2= 0.64, P = 0.01; Y2boys = –6.32 + 0.23 (age in years at GH start) + 1.75 [spinal RT (1 = yes; 2 = no)]; r2= 0.646; P < 0.01]. This small historical cohort underscores that final stature is significantly reduced when immature bones are exposed to ionizing radiation. Intramuscular vs. sc use of GHRx is likely to be simply a surrogate marker for earlier methods of treatment. Of note, spinal RT did not significantly impact girls’ final heights, whereas in boys, spinal RT strongly predicted ultimate short stature and a reduced response to GHRx. This sexually dichotomous response may be due in part to the greater percentage of spinal growth remaining for boys vs. girls throughout childhood.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
FINAL HEIGHT IN survivors of childhood head tumors is often less than expected based on midparental sex-adjusted target height (SATH). This reduction in final height is attributed to a variety of factors, including the impact of serious illness and poor nutrition, the direct impingement of the tumor on the hypothalamus or pituitary gland, and the effects of treatment of the tumor (1). Furthermore, GH deficiency (GHD) may occur as the result of a tumor’s direct effect on hypothalamic and pituitary structures or as the result of surgical or radiation treatment (2). Radiation therapy is an important component in the treatment of many tumors of the head, for primary tumors that may not be easily reached through conventional surgery, or for postsurgical ablation of residual tumor. Craniospinal radiation is included in therapeutic protocols when there is concern about metastasis throughout the central nervous system, particularly to the spinal column (3).

Although exogenous GH is frequently used to treat the resultant short stature, these patients are recognized to have great variability in their response to GH therapy (GHRx) (4, 5, 6, 7, 8, 9, 10). It is not clear which factors in a patient’s history and clinical course cause this variability. Therefore, we studied a historical cohort to ascertain the predictive factors prior to GHRx that may have influenced these patients’ post-GHRx final height.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
A chart review was performed on patients with a history of tumor of the head, who were treated with cranial or craniospinal radiation therapy and subsequently were treated with GH. This review was approved by the institutional review board of New York-Presbyterian Medical Center. Patients excluded were those who died, who had recurrence of their brain tumor before completion of growth, who were not yet at final height, or who failed to return for follow-up.

Two outcome measures were used for the efficacy of GHRx. First, to assess final height relative to genetic influence, final height for midparental SATH was measured as an SD score (SDS). This first outcome was termed Y1. Midparental SATH was computed as: [maternal height (centimeters) + paternal height (centimeters)]/2 + 13 cm (male) or – 13 cm (female), where absolute final height (centimeters) SDS was computed as a multiple of ±5 cm/SD for SATH (centimeters) (11). Second, to evaluate the change in SDS for height over the course of GHRx, we calculated any change by subtracting the final height SDS post-GHRx from the predicted height SDS pre-GHRx. This second outcome was termed Y2. Predicted height was calculated with the Adult Height Predictor (Genentech, Inc., South San Francisco, CA), using bone age, relation of bone age to chronological age, and present height (12, 13); final height SDS was calculated with the Palm Systems Height Predictor (Eli Lilly & Co., Indianapolis, IN) (14).

Statistics

Assessment of the impact of the following variables was performed for outcomes Y1 and Y2: sex, type of tumor diagnosed, weight at start of GH treatment (kilograms), height at start of GH treatment (centimeters), height at start of GH treatment (SDS), age at diagnosis of cancer (years), radiation dose during treatment (Gray), spinal radiation exposure during radiation treatment (yes or no), years treated with radiation, treatment with chemotherapy (yes or no), age at start of GH treatment (years), bone age at start of GH treatment (years), age at start of GH treatment minus bone age (years), GH formulation (im or sc), GH deficiency (yes or no), peak GH response to stimulation test (nanograms per milliliter), frequency of GH administration, initial GH dose (milligrams per kilogram per week), and gonadotropin agonist therapy or synthetic thyroid hormone replacement (yes or no). Multiple regression with stepwise selection of predictors meeting a value of P < 0.15 for entry into the model and a value of P < 0.15 for staying in the model was used to generate preliminary models. For each model generated, colinearity analysis among predictors, partial correlations, semipartial correlations, Akaike’s information criterion, and stepwise improvement in total model r were examined. Models with predictors with least colinearity, highest partial and semipartial correlations, and lowest Akaike’s information criterion were selected. Given the small sample size, subsequent models were restricted to the two best predictors.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The clinical parameters of the 19 patients who met inclusion criteria and were studied are shown in Table 1Go. Table 2Go summarizes initial and final height parameters. Both tables show parameters for girls and boys separately. Final outcomes were measured as the SDS for Y1, the difference of final height from midparental SATH, and Y2, the change from predicted height SDS to final height SDS.


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  		TABLE 1. Clinical parameters related to treatment of tumor and GHRx

 

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  		TABLE 2. Initial and final height parameters

 
For girls, Y1 best correlated with younger age at diagnosis and im vs. sc GHRx [Y1girls = –9.95 + 0.38 (age in years at diagnosis) + 3.11(GH method (1 = im; 2 = sc)]; r2 = 0.898; P = 0.02; Fig. 1AGo]. Y2 best correlated with delayed bone age and younger age at diagnosis [Y2girls = –3.54 + 1.8 (bone age – age in years) + 0.334 (age at diagnosis in years); r2= 0.956; P = 0.02; Fig. 1BGo]. For boys, spinal RT and younger age at diagnosis or treatment were associated with Y1 [Y1boys = –11.22 + 4.65 [spinal RT (1 = yes; 2 = no)] + 0.396 (age in years at diagnosis); r2= 0.64; P = 0.01; Fig. 2AGo], and Y2 [Y2boys = –6.32 + 0.23 (age in years at GH start) + 1.75 [spinal RT (1 = yes; 2 = no)]; r2= 0.646; P < 0.01; Fig. 2BGo].



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  		FIG. 1. Girls’ final heights.

 


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  		FIG. 2. Boys’ final heights.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Survivors of childhood tumors of the head who have received RT are known to have decreased final height. The degree to which final height is affected is variable, as is the response to GHRx, which is used to improve the resultant short stature. We therefore analyzed a cohort of survivors of tumors who were treated with cranial or craniospinal RT and were subsequently treated with GH to determine which treatment and demographic parameters had the greatest predictive value for growth response to GHRx.

GHD or a defect in GH secretion will diminish the potential for growth. All patients in our cohort either tested as GHD or were presumed to have a secretory defect after receiving high doses of cranial irradiation, with final height predictions significantly shorter than their predicted midparental SATHs, which account for height potential based on genetic factors (11). These findings are consistent with other studies demonstrating GHD after cranial RT of 18–25 Gy or more (1, 15, 16, 17, 18) within 1–2 yr after RT (19, 20), due to direct injury to hypothalamic neurons rather than damage to the pituitary itself (15, 20). In addition, a pattern of low growth velocity, despite a stimulated GH level of 6 ng/ml or more, has been suggested to signify a neurosecretory defect within the hypothalamus (21), particularly because IGF-I levels do not consistently discriminate between subjects with and without GHD (15).

Previous studies have attempted to correlate patient characteristics and treatment parameters with final height outcome. Chemotherapy has been associated with a variable risk of short stature (4, 22, 23, 24, 25, 26). Puberty has been noted to take place at a significantly younger age after RT, but does not significantly affect final height (4, 27), whereas delayed puberty has also been associated with decreased upper segment to lower segment ratio, presumably due to decreased sex steroid hormone production (5). Recent studies suggest that in the case of early puberty, the use of GnRH agonist therapy alone or in combination with GHRx may result in an improvement in final height in this population or in other cases of GHD (6, 28, 29, 30, 31).

Other parameters known to influence final height outcome in patients who have received GHRx include the patient’s genetically determined height potential (32), GHRx dose and frequency (22), and other concomitant hormone insufficiencies, such as hypothyroidism (33). Additionally, younger age at the time of RT has consistently been associated with a strong risk for short adult height (1, 25, 26, 34), as has treatment with RT during rapid pubertal growth (35). Similar to these studies, we showed in both boys and girls that irradiation had a significantly negative impact on final height with younger age. The additional negative effect of a delayed bone age seen in the girls’ cohort likely represents a biological surrogate marker for the risk factor of younger age. For girls, im administration of GH also significantly decreased the salutary effect of GHRx on final height. The reduced effect of semiweekly im vs. daily sc administered GHRx has previously been noted (36).

More than any other factor, however, irradiation of the spine has been implicated in a high risk of short adult height. This is probably due to damaged growth plates after high doses of radiation (37). Patients treated with spinal RT are consistently shorter than those treated with cranial RT alone (1, 7, 19, 25, 26, 35), with reduced response to GHRx or normal endogenous GH levels after spinal RT (8). The upper segment to lower segment ratio is decreased in all reviewed studies (5, 21, 38, 39, 40), with a greater negative effect on growth of spinal RT vs. cranial RT despite an overall final height improvement with GHRx (9, 38, 41, 42), whereas both final and sitting heights in children treated with cranial RT have been shown to improve with GHRx (10, 42).

The striking negative effect of spinal RT for boys, but not for girls, may be due to the difference between boys and girls in potential spinal growth. Growth curves of sitting height (43, 44) demonstrate that the percentage of height remaining is greater in boys than in girls at every age until final height and may be used to predict final height after RT (45). The median ages at the time of irradiation of our male and female cohorts were 5.3 and 5.5 yr, respectively. Using growth charts of sitting height, the median potential of spinal growth remaining at the time of RT was 31.3 cm for boys and 24.6 cm for girls, a difference of 6.7 cm. We therefore suggest that although this study included only a small and heterogeneous group of patients, sex-dependent growth may account for some of the significant difference between the responses of boys and girls to GHRx after spinal RT.

Conclusions

This small historical cohort underscores that radiation damage to less mature spines, as evidenced by younger age and delayed bone age, is highly correlated with greater loss of statural growth. We observed an effect of spinal irradiation on final height in our cohort of boys, but not in our cohort of girls. We suggest that this may reflect a significantly greater percentage of growth remaining for boys vs. girls of similar age until achievement of final height. We therefore support prior conclusions that a major contributing factor to loss of height despite GHRx is direct damage to growing bones. Furthermore, although we observed a sexually dichotomous response to treatment, we acknowledge that our groups had considerable heterogeneity, including different methods of radiation treatment. We therefore suggest that similar analyses of larger cohorts of similar patients are needed to verify the findings we observed in our small historical cohort.


   Footnotes
 
Abbreviations: GHD, GH deficiency; GHRx, GH treatment; RT, radiation therapy; SATH, sex-adjusted target height; SDS, SD score.

Received July 30, 2004.

Accepted September 23, 2004.


   References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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