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ELECTRONIC ARTICLE |
* Department of Pediatrics, Dalhousie University
Department of Psychology
Perinatal Epidemiology Research Unit
|| Department of Nursing, IWK Health Centre, Halifax, Nova Scotia, Canada
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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Methods. A population-based cohort of very preterm infants who were born to mothers who resided in Nova Scotia or Prince Edward Island were evaluated at 4, 8, 12, and 18 months’ corrected gestational age, which included a CAT/CLAMS by a physician. At 18 months’ corrected gestational age, each child was assessed using the Bayley Scales of Infant Development II, the "gold standard" for developmental delay in young infants. The results of each CAT/CLAMS was compared with the 18-month MDI to identify significant developmental delay (MDI <70).
Results. Optimal scores on the CAT/CLAMS to identify correctly MDI <70 were determined by using the 
statistic for chance independent agreement. Sensitivities and specificities for optimal cutoff scores were as follows: 4-month score <109 (88% and 37%), 8-month score <98 (75% and 82%), 12-month score <81 (63% and 99%), and 18-month score <83 (88% and 98%).
Conclusion. Sensitivity and specificity of the CAT/CLAMS are high in very preterm infants at identifying major developmental delay at 12 and 18 months. For follow-up programs without psychology services, the CAT/CLAMS at 12 and 18 months is a reasonable screening tool to determine which children need expedited psychology referral for cognitive delay.
Key Words: developmental screening • preterm infants • Capute scales • neurodevelopmental outcome
Abbreviations: MDI, Mental Developmental Index • PFUP, Perinatal Follow-Up Program • CAT/CLAMS, Cognitive Adaptive Test/Clinical Linguistic and Auditory Milestone Scale • BSID, Bayley Scales of Infant Development • LMP, last menstrual period
The rate of severe cognitive delay (Mental Developmental Index [MDI] <70) at 18 months’ corrected gestational age in infants <31 weeks’ gestational age, as based on data from the Perinatal Follow-Up Program (PFUP) of Nova Scotia 1997–1999, is 10.7%. In a meta-analysis, Lorenz et al1 noted rates of developmental delay as high as 23% for the extremely immature infant. With such high rates of developmental delay, it is essential that good screening tools be available to identify cognitive delay. One such tool is the Cognitive Adaptive Test/Clinical Linguistic and Auditory Milestone Scale (CAT/CLAMS), which was developed >20 years ago.2 The CAT/CLAMS is a simple screening tool for pediatricians to learn and generally takes <10 minutes to administer, even by pediatric residents.3 Correlation coefficients comparing the CAT/CLAMS index score with the Bayley Scales of Infant Development II (BSID-II) MDI have been reported to be as high as 95%,4 with sensitivities for identifying MDI <70 to be 88%4 and specificity to be 97%.5
It has been suggested that the pediatrician is in an important position to conduct early screening of children for developmental delay so that appropriate early intervention services can be initiated.6 In addition, the American Academy of Pediatrics has recommended that pediatricians acquire skills in administering and interpreting reliable and valid developmental screening tools.7
Previous research has evaluated the CAT/CLAMS for (1) children with suspected developmental delay,4,8,9 (2) follow-up for infants who recovered from aseptic meningitis,10 (3) the evaluation of normal infants recruited from a well-infant clinic,11 and (4) a high-risk follow-up clinic.5 The results obtained from a high-risk follow-up clinic prompted us to examine our own experience of using the CAT/CLAMS in a follow-up population. Despite that Macias et al5 identified their population as being randomly selected from a consecutively enrolled cohort that had a mean gestational age of 31 weeks and a mean birth weight of 1694 g in their follow-up clinic, it is unclear whether the inception cohort was from a population-based cohort or there were any specific enrollment criteria for their follow-up clinic.
Macias et al5 noted in their work 2 additional features that are addressed further in this article: (1) an older age at performing the CAT/CLAMS is more predictive for the MDI on the BSID-II, and 2) CAT/CLAMS index scores are not equivalent to the MDI scores. Macias showed that using a higher cutoff score on the CAT/CLAMS resulted in a greater sensitivity with little loss in specificity at predicting MDI scores <70.
The objective of the present study was to determine the optimal age to perform the CAT/CLAMS and the optimal "cutoff" score to identify a birth cohort of infants of <31 weeks with MDI scores <70. Once cutoff scores are determined, the sensitivity, specificity, and likelihood ratios are ascertained for these scores.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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70%) of the 18-month CAT/CLAMS scores were conducted in a similarly blinded manner. The total composite CAT/CLAMS score was determined by the age-equivalent level of function divided by the corrected gestational age multiplied by 100 to give an index score as recommended by Capute and Accardo.12,13 Thus, if the child was functioning at his or her exact corrected gestational age, then the score would be 100. Gestational age was assigned on the basis of 1 of the following 3 criteria: conception date, last menstrual period (LMP), early ultrasound, or a clinical assessment (either a Ballard assessment14 performed by the housestaff or clinical estimate performed by the attending neonatologist). The conception date was used over all other estimates, but this was available in only 4% of preterm infants. The ultrasound dates were used over the LMP when the difference between the ultrasound and the LMP was >10 days as suggested by Gray et al15; otherwise, dates were used. When no maternal dates were available, ultrasound was used. The only time a Ballard score or other clinical assessment was used is when no other reliable dating was available.
At 18 months’ corrected gestational age, the developmental psychologist administered the BSID-II, to assess for cognitive delay, which was considered the "gold standard." By comparing each child’s CAT/CLAMS score with the MDI at 18 months’ corrected gestational age, receiver operator curves were constructed for each age (4, 8, 12, and 18 months’ corrected age) to estimate the area under the curve. To determine the optimal CAT/CLAMS score that predicted an MDI <70, the statistic measuring chance independent agreement between the CAT/CLAMS and the MDI <70 was calculated for each CAT/CLAMS score, and the highest was used.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Of the 172 infants who were included in the study, 147 (85% of the eligible population) had both an MDI of the BSID-II conducted by a developmental psychologist and a CAT/CLAMS conducted by the physician at 18 months’ corrected gestational age. Eight had only the CAT/CLAMS (median score: 91; range: 63–104), 4 had only the MDI (median score: 82; range: 67–103), and 13 had neither. Of the 13 with neither score, 4 had scores for both performed at 24 months, and 3 would have been identified correctly as normal and 1 incorrectly would have been called abnormal (false positive). One other child had a normal CAT/CLAMS at 24 months and a normal Differential Ability Scales at 3 years, and 1 other child had such severe disability from cerebral palsy that the MDI was impossible to obtain. None of these additional results would have had a significant impact on the 18-month outcomes noted in Table 2.
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statistic were <109 at 4 months, <98 at 8 months, <82 at 12 months, and <84 at 18 months. These values concurred with visual inspection of the receiver operator curves. Table 2 confirms that 12 and 18 months have the highest likelihood ratios for a positive test with the lowest values for a negative test; therefore, they are the best ages to identify the MDI score <70.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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8 to 9 points higher than the BSID-II.16 An area of ongoing controversy that may affect the interpretation of the current data is correction for prematurity. Some investigators stop correcting after 2 years,17 whereas others continue until 8.5 years.18 It might be argued that for infants at 4 and 8 months’ corrected age, there is a proportionally greater degree of age correction, making the CAT/CLAMS scores "overcorrected." This may explain, to some extent, why CAT/CLAMS scores at these ages are poor predictors of the 18-month MDI. We found at 4 months’ corrected age that an uncorrected CAT/CLAMS score of 61 performed marginally better than the corrected scores with a sensitivity of 71% and a specificity of 63% at predicting the 18-month MDI <70. This was not true at other ages.
Another issue to be considered is that the derivation of the CAT/CLAMS and the MDI scores is different. The CAT/CLAMS score is a simple ratio of the developmental age level ÷ corrected age x 100, whereas the MDI of the BSID is indexed to a Gaussian distribution so that 1 SD about a mean score of 100 is ±15 points. This means that a score of 85 for a child of 18 months (16th percentile) would be a developmental level of 16 months, whereas a score of 70 (2nd percentile) would be 14 months. The CAT/CLAMS scores at these developmental performances would be 89 and 78, respectively. Use of the receiver operator curve allows us to identify the "optimal" CAT/CLAMS score to predict the MDI <70 (Fig 1).
A minor limitation of the present data is that a small number (14%) of CAT/CLAMS scores at 18 months were derived from the items performed by the developmental psychologist on the same day, which are in common with the BSID-II. To address this issue, we changed the schedule of testing so that the CAT/CLAMS was performed 2 weeks after the BSID-II. An additional refinement by this separation was that all physicians remained blinded to MDI scores until the CAT/CLAMS was performed.
Our study performed much better than Macias et al,5 who found a very low sensitivity and a very high specificity when using the CAT/CLAMS as a screening tool to identify infants who have MDI scores <70. Our population confirmed the high specificity of the CAT/CLAMS; however, we also noted a relatively high sensitivity at 12 and 18 months’ corrected gestational age in contrast to data by Macias et al. We found a similar trend of improved predictability of performing the CAT/CLAMS at higher ages at identifying children with developmental delay (see Table 2). In addition, the data of Macias et al suggested that a score of 70 on the CAT/CLAMS may not be optimal at identifying children with MDI scores <70, an observation supported by Capute et al,19 who examined the ability of an earlier version of the CLAMS component in which a score of 80 on the CLAMS was comparable to 70 on the MDI. We took this 1 step further by determining the test characteristics of the "optimal" scores at various ages of the CAT/CLAMS at identifying MDI score <70 at 18 months’ corrected age. Our data suggested that the CAT/CLAMS tends to score higher than the MDI such that it did not make sense to assume that the CAT/CLAMS <70 was best at predicting the MDI <70. If we had done so at 18 months, then the sensitivity would be only 56% with a specificity of 100%. The linear regression curve (r2 = 0.74) of the 18-month CAT/CLAMS for the 18-month MDI is MDI18 = 0.9 x CAT/CLAMS18 – 2.4, where MDI18 is the 18-month corrected age MDI score and CAT/CLAMS18 is the 18-month corrected age CAT/CLAMS score. Therefore, the CAT/CLAMS score is 10% higher than the corresponding MDI score. It was not the intent of this study to adjust the MDI score for variables other than the CAT/CLAMS; however, in addition to the 18-month CAT/CLAMS, temperature on admission to the NICU accounted for a small amount of variance when entered in an adjusted model. Admission temperature adjusted the MDI downward by 4 points for every degree below 37°C.
To summarize the performance at the 2 optimal ages, the CAT/CLAMS at 12 months moves the pretest probability of 10.7% (as in our population) to a posttest probability of 78% when the score is <82 or to a posttest probability of 4% when the score 
82. At 18 months, the posttest probability moves to 81% when the CAT/CLAMS score is <84 or to 2% when the CAT/CLAMS is 84.
We believe that the CAT/CLAMS may be beneficial to some follow-up programs that do not have access to developmental psychology services on a routine basis. With the use of this simple tool, the majority of infants with developmental delay can be identified and thus give the physician the rationale for an expedited referral to a psychologist. It is also very useful when the CAT/CLAMS score is normal because this allows the physician to be reassuring to the family with regard to early cognitive delay.
Another aspect for some programs without psychology services is whether the economics justifies hiring a psychologist to provide a diagnostic service for developmental delay in the preterm infant. As an example, in Nova Scotia, the psychologist usually takes 2 hours to perform and interpret the BSID-II at 18 months’ corrected age. For infants <31 weeks, there are 60 such assessments per year. At conservative private rates of $500 (Canadian) per BSID assessment, the total annual expenditure of $30000 would be required for this service. On the basis of the data presented in this study, it is estimated that the physician could reduce the need from 60 psychology referrals per year to 10, costing $5000 per year (10 x $500). There may be a slight increase in physician time spent preforming the CAT/CLAMS; however, most follow-up physicians conduct a developmental assessment but generally not a standardized tool such as the CAT/CLAMS. By substituting the time spent performing a nonstandardized tool with the CAT/CLAMS, the cost for additional physician time is insignificant.
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FOOTNOTES |
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Address correspondence to Michael J. Vincer, MD, IWK Health Centre, 5850/5980 University Ave, PO Box 9700, Halifax, Nova Scotia, Canada, B3K 6R8. E-mail: vincer{at}dal.ca
No conflict of interest declared.
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This article has been cited by other articles:
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  R. G. Voigt, A. M. Llorente, C. L. Jensen, J. K. Fraley, W. J. Barbaresi, and W. C. Heird Comparison of the Validity of Direct Pediatric Developmental Evaluation Versus Developmental Screening by Parent Report Clinical Pediatrics, July 1, 2007; 46(6): 523 - 529. [Abstract] [PDF]
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