Journal of Pediatric Surgery (2007) 42, 1052 – 1056
www.elsevier.com/locate/jpedsurg
Approaches to neurodevelopmental assessment in congenital diaphragmatic hernia survivors Catherine Chena,*, Sandra Friedmanb, Samantha Butlerb, Stefanie Jerussc, Norma Terrinc, Hocine Tighiouartc, Janice Wareb, Jay M. Wilsona, Susan K. Parsonsc a
Department of Surgery, Children’s Hospital, Boston, MA 02115, USA Department of Medicine, Children’s Hospital, Boston, MA 02115, USA c Institute for Clinical Research and Health Policy Studies, Tufts-New England Medical Center, Boston, MA 02111, USA b
Index words: Neurodevelopmental outcome; Pediatric surgery; Congenital diaphragmatic hernia; Bayley Scales of Infant Development-II; Developmental Profile-II
Abstract Background: Infants with congenital diaphragmatic hernia require complex surgical care and may have neurodevelopmental morbidity. We examined the performance of reports of motor functioning in 25 congenital diaphragmatic hernia survivors using the parent-completed Developmental Profile-II and a clinical evaluation by a neurodevelopmental pediatrician (MD) measured against the Bayley motor scale. Methods: Bayley motor scores were dichotomized as normal or abnormal. Sensitivity and specificity were calculated for each test. Results: The median age at assessment was 25 months. Bayley motor scores were abnormal in 77% of infants tested (10/13). The MD examinations detected motor problems in 92% (12/13). Sensitivity and specificity of the MD examination were 1.0 and 0.33, respectively. Developmental Profile-II physical scores were abnormal in 15% (2/13); sensitivity and specificity were 0.2 and 1.0, respectively. Conclusions: The high rate of abnormal motor findings in this study supports the need for ongoing screening and evaluation. The sensitivity of MD examinations was excellent, but hypotonia findings were not universally corroborated by the Bayley. Although specificity of parent-reported motor findings was high, parents underreported abnormal motor findings. Parental reports of neurodevelopmental problems should be heeded, and physicians should perform screening motor examinations. Bayley assessments may be warranted to determine the functional implications of observed abnormalities. D 2007 Elsevier Inc. All rights reserved.
Congenital diaphragmatic hernia (CDH) is a congenital malformation of an incompletely formed diaphragm, requiring surgical repair as a neonate. In addition to pulmonary hypoplasia, neonates with CDH may also have associated
Papers presented at the 58th Annual Meeting of the Section on Surgery of the American Academy of Pediatrics. * Corresponding author. Tel.: +1 617 355 0535; fax: +1 617 730 0298. E-mail address:
[email protected] (C. Chen). 0022-3468/$ – see front matter D 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jpedsurg.2007.01.042
cardiac anomalies, pulmonary hypertension, or other genetic syndromes, which complicate their postnatal management. The complexity of care often required in the peri- and postoperative period for CDH patients renders CDH the most expensive of any pediatric surgical condition based on the number of diagnosis related group units [1]. Congenital diaphragmatic hernia survivors have been reported to experience ongoing medical morbidity, including pulmonary and nutritional morbidity, and gastroesophageal reflux [2-4]. In case series of CDH survivors treated with neo-
Approaches to neurodevelopmental assessment in CDH survivors natal extracorporeal membrane oxygenation (ECMO), difficulties with developmental delay, hearing loss, and musculoskeletal development have been described [5,6]. We have found that a subset of long-term CDH survivors with ongoing clinical problems a median of 8 years after surgery has lower functional status [7]. In addition, family impact is profound and long-standing for this subset of CDH survivors with more severe conditions and ongoing morbidity (Chen et al, unpublished data). The CDH population provides a unique model of a complex pediatric surgical condition, which has become a paradigm of chronic disease. Few studies have reported the neurodevelopmental outcomes of CDH survivors in the contemporary era since 2000, when in-hospital survival has been reported to be greater than 90% at several institutions [8,9]. In this pilot study, we examined 3 independent approaches to neurodevelopmental assessment of young CDH survivors, focusing on motor functioning. We evaluated the performance of reports of motor functioning using 2 screening measures, the parent-completed Developmental Profile-II (DP-II) and a clinical evaluation by a neurodevelopmental pediatrician (MD), measured against the diagnostic Bayley motor scale administered by a psychologist.
1. Methods 1.1. Patient selection and data collection We identified 68 patients with CDH who survived surgical repair to hospital discharge at Children’s Hospital Boston from January 1, 2000 through December 31, 2003. The in-hospital survival rate during this period was 87%. Patients were excluded from this Institutional Review Board approved study (#X03-02-009) if they received preoperative or postoperative care at Children’s Hospital Boston but underwent surgical repair of CDH at another institution. Of the 68 survivors, 19 patients could not be reached, either by mail or by telephone, or via an identifiable primary care physician. The evaluable cohort of 49 patients was recruited by mail to participate in this study and asked to return an opt-out postcard to provide consent. Twenty-five patients participated in this pilot study. Reasons cited for nonparticipation included bnot interestedQ for 8 patients, btoo much to participateQ for 6 patients, and bwould if asked at a different timeQ for 1 patient. Perinatal and perioperative data were obtained for the cohort of 68 established CDH survivors by review of hospital medical records. Medical issues at the time of hospital discharge and at the time of the study were defined by the presence of any of the following: cardiac issues (need for diuretics, inotropes, or antihypertensive medications); pulmonary issues (need for bronchodilators, steroids, or home oxygen therapy); or gastrointestinal issues (need for parenteral nutrition, gastrostomy tube feeds, or medications for gastroesophageal reflux).
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1.2. Study instruments and assessments Three independent approaches to neurodevelopmental assessment of motor functioning were used in this study. 1.2.1. Parent report All 25 study participants completed the DP-II, a normreferenced developmental screening measure administered as a structured interview (by author S.J.) that asks parents to estimate their child’s current level of functioning [10]. The DP-II contains 217 developmental tasks for the age range from birth to 12 years and addresses 5 functional domains: physical, adaptive, social, academic, and communication. Domain scores are obtained using established scoring algorithms and are interpreted in terms of the degree of developmental lag between chronological age and current levels of functioning. Norm tables are used to determine the significance of lags. This study focused on the DP-II physical domain score as a measure of parent-reported motor functioning. Delayed or borderline delayed DP-II physical scores were classified as dabnormal.T 1.2.2. Physician’s clinical evaluation Twenty-three study participants received a clinical evaluation by a neurodevelopmental pediatrician (author S.F.; referred herein as MD) as part of their routine follow-up in the CDH Outpatient Multidisciplinary Clinic (referred herein as CDH Clinic). Two patients did not see the MD at a time compatible with the DP-II interview or the Bayley assessment. Clinic notes were extracted, and motor findings on physical examination, if any, were tabulated for each patient. 1.2.3. Bayley Scales of Infant Development-II Thirteen study participants provided consent and completed the psychologist-administered (author S.B.)-administered diagnostic Bayley Scales of Infant Development-II, which was used as our gold standard. The Bayley Scales of Infant Development-II measures mental and motor development and tests the behavior of infants from 1 to 42 months of age [11]. Twelve patients did not consent to the Bayley, which was obtained for research purposes in this study and not referred based on clinical examinations. This study focused on the motor scale, which assesses the degree of body control, large muscle coordination, fine motor skills of the hands and fingers, dynamic movement, postural imitation, and stereognosis. Bayley motor scores were obtained using established scoring algorithms and compared with age appropriate norms. Scores were further dichotomized as normal or abnormal by the psychologist. Abnormal scores reflect those classified as bmildly delayed performanceQ (score range, 70-84) or bsignificantly delayedQ (score below 69).
1.3. Statistical analysis Summary statistics were calculated for each outcome variable, and descriptive results were summarized for each cohort tested. Sensitivity and specificity were calculated for
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each test, as measured against the gold standard Bayley motor scale.
2. Results 2.1. Characteristics of study participants versus nonparticipants
2.2. Patient and clinical characteristics
Study participants did not differ from non-participants by gestational age, birth weight, Apgar at 5 minutes, hernia type and location, presence of cardiac or genetic anomalies, need for ventilator management, time on ventilator, need for Table 1
Patient and clinical characteristics
I. Patient information at time of study Median age of child in mo (range) % Male % With current medical issues at time of study* II. Clinical data at time of surgery Mean gestational age in wk (SD) Mean birth weight in kg (SD) Median Apgar at 5 min (range) Hernia type % Bochdalek % Morgagni Hernia location % Left % Right % Bilateral % Cardiac anomalies % Congenital malformations/genetic syndromes % Requiring ICU stay Median ICU LOS in d (range) % Requiring ventilator management Median vent time in d (range) % Requiring ECMO Median ECMO time in h (range) Median hospital LOS in d (range) % With medical issues at time of discharge * P b .05.
In study (n = 25)
Yes Bayley No Bayley (n = 13) (n = 12)
25.0 (8.0-49.0) 60.0 72.0
19.0 (8.0-40.0) 61.5 92.3
32.0 (11.0-49.0) 58.3 50.0
37.7 (2.3)
37.6 (1.6)
37.8 (2.9)
3.1 (0.6)
3.0 (0.5)
3.1 (0.7)
7 (1-9)
7 (1-9)
92.0 8.0 72.0 24.0 4.0 12.0 32.0
100 0 61.5 38.5 0 7.7 30.8
ECMO, ECMO time, need for intensive care unit (ICU) stay, ICU length of stay (LOS), or hospital LOS (data not shown). Compared with study nonparticipants, a greater percentage of participants had medical issues at the time of hospital discharge (100% vs 72.1%; P b .0001).
8 (5-9)
83.3 16.7 83.3 8.3 8.3 16.7 33.3
Table 1 summarizes the patient and clinical characteristics of the 25 study participants, and compares the subset of 13 patients who completed a Bayley assessment with the 12 who did not. The median age of participants at the time of the study was 25 months (range, 8-49 months). All 25 study participants (100%) had medical issues at the time of initial hospital discharge. At the time of the study, 72% of study participants had current medical issues. Those patients who completed a Bayley assessment had a higher percentage of current medical issues compared with those who did not complete a Bayley (92.3% vs 50%; P = .011). Patients who completed a Bayley did not differ significantly by any other neonatal or perioperative characteristics compared with those who did not complete a Bayley (Table 1).
2.3. Neurodevelopmental assessment of motor functioning The proportion of motor abnormalities differed by source. Table 2 shows that Bayley motor scores were abnormal in 77% of infants tested (10/13), whereas MDdetected abnormal motor findings were seen in 92% of the same cohort of children (12/13). The sensitivity and specificity of the MD examination were 1.0 and 0.33, respectively. The DP-II physical scores were abnormal in 15% of this cohort (2/13), with a sensitivity and specificity of 0.2 and 1.0, respectively. For the entire cohort evaluated by the MD, 10 of whom did not undergo Bayley assessment, MD examinations detected motor findings in 83% of children (19/23) in contrast with the abnormal parentreported DP-II physical score in 22% (5/23).
3. Discussion 100 17.5 (1.0-64.0) 96.0
100 22.0 (7.0-60.0) 100
100 17.0 (1.0-64.0) 91.7
15.5 (5.0-55.0) 32.0 233.5 (130-504) 46.5 (7.0-295) 100
14.0 (5.0-55.0) 46.2 257.5 (198-504) 53.0 (26-295) 100
16.0 (6.0-51.0) 16.7 149 (130-168) 35 (7-145) 100
In the contemporary era of surgical care of CDH patients since 2000, improved survival rates at many North American centers have led to possible concern about increasing numbers of CDH survivors with ongoing medical morbidity. The potential for additional neurodevelopmental sequelae remains a true risk, which may translate to decreased functional status and the development of learning disabilities requiring special educational services. Our previous studies have shown that a subset of CDH survivors with a median age of 8 who have ongoing and more severe medical problems have significantly lower functional status scores [7]. In our retrospective review of this older cohort of patients, family recall of early intervention (EI) referral and enrollment in EI services
Approaches to neurodevelopmental assessment in CDH survivors Table 2
Summary of motor findings in 13 patients who completed the Bayleya
Patient
Age (mo)
1 2 3 4 5 6 7 8 9 10 11 12 13
24 36 40 29 31 26 16 16 12 12 13 9 8
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Sex
Abnormal Bayley motor score
MD-detected motor findings
DP-II physical scoreb
Medical problemsc at time of study
Female Female Female Female Male Male Male Male Male Male Male Female Male
Yes Yes No No Yes Yes No Yes Yes Yes Yes Yes Yes
Hypotonia Hypotonia/Asymmetry None Hypotonia/Motor delays Motor delays Hypotonia/Fine motor problems Hypotonia Hypotonia Motor delays Hypotonia/Asymmetry/Motor delays Fine motor problems Motor delays Hypotonia/Motor delays
Normal Normal Normal Normal Delayed Normal Normal Normal Normal Normal Normal Borderline delayed Normal
Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes Yes Yes
a
Considered to be gold standard for evaluation of neurodevelopmental issues, performed by psychologist. Delayed or borderline delayed scored as abnormal. c Medical problems defined by the presence of any of the following: cardiac issues (need for diuretics, inotropes, or antihypertensive medications), pulmonary issues (need for bronchodilators, steroids, or home oxygen therapy), or gastrointestinal issues (need for parenteral nutrition, gastrostomy tube feeds, or medications for gastroesophageal reflux). b
was surprisingly low at 57% and 48% of the population, respectively [7]. The underlying premise of our current studies is that earlier detection of neurodevelopmental deficits may allow for earlier intervention and support. Patients with CDH at Boston Children’s Hospital are routinely referred for evaluation by EI programs at the time of hospital discharge. Longitudinal studies are required to assess whether these interventions have an impact on neurodevelopmental outcomes in CDH patients. To begin to understand the neurodevelopmental outcomes of this cohort of contemporary CDH survivors, we evaluated the performance of reports of motor functioning using 3 independent approaches, comparing parent report and clinical evaluation by a neurodevelopmental pediatrician with the gold standard Bayley motor scale. We chose to focus on motor functioning at this young age, rather than language abilities, because of its developmental appropriateness and the ease of motor measurement. More importantly, the various approaches to early detection of neurodevelopmental concerns have different costs and benefits associated with each. Although the use of parents’ reports is the least costly in terms of administration and interpretation [12], these parent reports of child capabilities are often considered unreliable. In addition, although parents may be concerned about their child’s development, it may be unclear whether concerns indicate actual developmental problems. Glascoe et al [13] showed in a pilot study that although parents’ concerns about their children’s development took the form of value judgments, they could be classified into accepted developmental domains and related to performance on screening test. Finally, evaluations by a neurodevelopmental pediatrician or a Bayley assessment by a trained psychologist may not be as readily or universally accessible to all CDH patients as they are at Children’s Hospital Boston.
Compared with the diagnostic Bayley motor scale, which we used as our gold standard, we found that the sensitivity of MD clinical examinations was excellent (1.0), but MD examinations also reported motor issues not corroborated by the Bayley (specificity, 0.33). This difference represents findings from 2 patients. The MDdetected finding of hypotonia was rated as abnormal but does not necessarily represent motor delays. In fact, 1 of the 2 patients in whom there was a difference between the MD and Bayley findings was found to be hypotonic but without motor delays. In addition, some abnormal motor findings on neurologic examination may not be reflected in functional deficits as identified by the Bayley. In our CDH Clinic, the MD examination is used as a screen to recommend further assessment and/or services, which is favorably reflected by the high sensitivity. The results of this pilot study will need further corroboration in a larger study, although the findings endorse the importance of thorough screening procedures. The use of the Bayley or other diagnostic motor testing may provide additional information about functional motor abilities. In contrast with MD examinations, parental reports of motor abnormalities using the DP-II were confirmed by the Bayley (specificity, 1.0) but were associated with underreporting of abnormal motor findings (sensitivity, 0.2). This finding may reflect the questionable use of the DP-II Physical scale as a developmental screening tool in our CDH population. However, when the DP-II Physical scale did detect a motor delay, the Bayley did corroborate the functional implications of these motor abnormalities. We conclude that parental reports of motor problems should be heeded by physicians, who should perform focused motor examinations in CDH survivors to identify all children who are at risk.
1056 The modest sample size of our pilot study mandates the need for further corroboration in a larger study. At Children’s Hospital Boston, patients with CDH are followed by an MD in the CDH Clinic and are referred for Bayley assessment when deemed necessary. Children determined to have delayed or abnormal development are referred for services and interventions both within and outside the hospital. In lieu of the neurodevelopmental MD follow-up, which may not be as accessible at other institutions, the use of other parent-reported developmental screening measures, such as the DP-II, in detecting neurodevelopmental problems will need to be evaluated. Yet another alternative is the use of parents’ concerns as a prescreening technique for identifying a subset of children in need of more in-depth developmental screening [12]. Parents’ concerns are elicited by the MD in the CDH Clinic, and future work will address whether these concerns can serve as a screening measure for neurodevelopmental disabilities.
Acknowledgments The authors thank Jocelyn Chapman, BS, for help with the acquisition of perinatal and perioperative data. This study was supported by a Faculty Career Development Fellowship Award from Children’s Hospital and the 50th Anniversary Program for Scholars in Medicine, Harvard Medical School (C.C.).
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Discussion Dr Eric Scaife (Salt Lake City, UT): Did you look at the subset of children who were salvaged with ECMO to see if their neuromotor development problems were more severe? Dr Chen (response): We did not specifically look at that group outside of the large cohort. Thirty-two percent of the entire group underwent ECMO. Dr Thomas Pranikoff (Winston-Salem, NC): Have you changed your assessment in your CDH clinic because of the results of this? Dr Chen (response): Actually not. There has always been a neurodevelopmental pediatrician involved in the multidisciplinary clinic since it was established in 1997. She considers her role as actually a screening tool. When she detects abnormalities on her physical exam, she makes a recommendation for further diagnostic testing. So, this has actually been occurring at our center for quite some time.
