MR Spectroscopic Evaluation of Psychomotor Delay of Unknown Cause in Children
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1 Pediatric Imaging Original Research Koşucu et al. MR Spectroscopy of Psychomotor Delay Pediatric Imaging Original Research Polat Koşucu 1 Sema Erdemli 2 Müjgan Sönmez 3 Sibel Kul 1 Ayşe Aksoy 3 Koşucu P, Erdemli S, Sönmez M, Kul S, Aksoy A Keywords: MR spectroscopy, psychomotor delay DOI: /AJR Received June 18, 2009; accepted after revision September 18, Department of Radiology, Medical School of Karadeniz Technical University, Farabi Hospital, 61080, Trabzon, Turkey. Address correspondence to P. Koşucu. 2 Department of Radiology, Numune Hospital, Trabzon, Turkey. 3 Department of Pediatry, Division of Pediatric Neurology, Medical School of Karadeniz Technical University, Farabi Hospital, Trabzon, Turkey. AJR 2010; 194: X/10/ American Roentgen Ray Society MR Spectroscopic Evaluation of Psychomotor Delay of Unknown Cause in Children OBJECTIVE. The aim of this study was to use MR spectroscopy to determine whether the brain metabolism of children with psychomotor delay of unknown cause differs from that of children without psychomotor delay. SUBJECTS AND METHODS. Twenty children (10 girls, 10 boys; mean age, 8.65 years; range, 4 15 years) with psychomotor delay and 19 children without psychomotor delay who served as controls (nine girls, 10 boys; mean age, 8.79 years; range, 6 13 years) were evaluated with multivoxel MR spectroscopy of the brain. The Stanford-Binet test and Wechsler Intelligence Scale for Children Revised were used to evaluate developmental quotient. Psychomotor delay was assessed as severe (developmental quotient, < 50), moderate (developmental quotient, 50 75) and mild (developmental quotient, > 75). The controls had a developmental quotient greater than 95. Spectra were acquired from eight specific voxels at the bilateral parasagittal frontal and parietal gray matter and the bilateral frontal and parietal white matter at the level of the centrum semiovale. The ratios of N-acetylaspartate (NAA) to choline (Cho), NAA to creatine (Cr), and choline to creatine were determined. RESULTS. Thirteen children had minor and seven children had moderate psychomotor delay. In the psychomotor delay group, the right frontal white matter NAA/Cho, NAA/Cr, and Cho/Cr ratios were 1.45 ± 0.18, 1.95 ± 0.33, and 1.36 ± 0.27; in the control group the ratios were 1.46 ± 0.23, 2.04 ± 0.33, and 1.41 ± The ratios for the left frontal lobe white matter were 1.34 ± 0.21, 2.01 ± 0.33, and 1.55 ± 0.26 in the psychomotor delay group and 1.42 ± 0.15, 2.17 ± 0.34, and 1.53 ± 0.25 in the control group. The ratios for the right parietal lobe white matter were 1.80 ± 0.38, 2.04 ± 0.43, and 1.18 ± 0.35 in the psychomotor delay group and 1.89 ± 0.31, 2.16 ± 0.30, and 1.17 ± 0.23 in the control group. The left parietal lobe white matter ratios were 1.66 ± 0.36, 2.08 ± 0.35, and 1.35 ± 0.29 in the psychomotor delay group and 1.81 ± 0.29, 2.17 ± 0.35, and 1.22 ± 0.26 in the control group. CONCLUSION. Metabolite distribution varied with brain region in children with and those without psychomotor delay. No significant difference was found between the brain metabolite ratios of children with psychomotor delay of unknown cause and those of agematched children without psychomotor delay. P sychomotor delay is a common socioeconomic problem among children, having a prevalence of 1 2%. A small percentage of these children have severe psychomotor delay, but most have mild delay [1]. With current diagnostic methods, the definitive cause of psychomotor delay cannot be discerned in 58 78% of children with mild and 23 43% of children with severe delay [1]. Clinicians and the families of children with psychomotor delay are frequently disappointed by the lack of neuroradiologic correlation, especially when the treatment alternatives and the long-term prognosis are considered [1]. MR spectroscopy (MRS) is a noninvasive technique by which metabolites in the brain are measured and information about structure, maturation, and disorders is obtained. Changes in levels of metabolites, such as N- acetylaspartate (NAA), choline (Cho), creatine (Cr), and lactate can be determined spectrally in a brain volume. Several investigators [2 6] have used MRS to evaluate changes in cerebral metabolism during normal brain maturation and white matter myelination. MRS also has proved useful for assessment of developmental delay; neurodegenerative, inflammatory, metabolic, and neuropsychiatric disorders; phakomatosis; 1110 AJR:194, April 2010
2 MR Spectroscopy of Psychomotor Delay hypoxic ischemic brain injury; and epilepsy [7 12]. For detecting a difference in the brain metabolism of children with psychomotor delay of unknown cause when no MRI abnormalities have been found, MRS can be used to elucidate the cause of the delay, contribute to determination of the long-term functional outcome for these children, and be included in the diagnostic algorithm as part of the neuroradiologic assessment. The aim of this study was to use MRS to determine whether the brain metabolism of children with psychomotor delay of unknown cause differs from that of children without delay. Subjects and Methods Case Selection Children evaluated for learning difficulties, failure to speak, failure in school, and amnesia in the pediatric neurology section of our hospital from February through December 2007 underwent the Stanford-Binet test if they were 3 6 years old and the Wechsler Intelligence Scale for Children Revised test if they were 6 15 years old. The results were used to determine developmental quotient (DQ). Psychomotor delay was assessed as severe (DQ, < 50), moderate (DQ, 50 75), or mild (DQ, > 75). Children with a DQ greater than 95 composed the control group [1]. The study was approved by the ethical committee. Informed consent was obtained from the parents or guardians of all patients. A total of 20 children (10 girls, 10 boys; mean age, 8.65 years; range, 4 15 years) without neuroradiologic abnormalities, cerebral palsy, chromosomal abnormalities, metabolic disease, epilepsy, autism, or other neurologic and degenerative disorders but who had mild or moderate psychomotor delay of unknown cause were included in the study. The control group consisted of 19 children without psychomotor delay (nine girls, 10 boys; mean age, 8.79 years; range, 6 13 years) who were evaluated by physical examination, psychomotor tests, and MRI. None of the children had evidence of disruptive behavior disorder not otherwise specified or attention deficit hyperactivity disorder according to the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition criteria or any signs of intracranial pathologic changes detected with MRI. Children with epilepsy or EEG abnormalities were excluded from the study. None of the patients received sedation during the MRS evaluation. Proton MRS Multivoxel MRS (TR/TE, 1,500/135) was performed on all patients with a standard head coil and 1.5-T MRI system (Magnetom Symphony, Siemens Healthcare). Three orthogonal baseline images were obtained with automated magnetic field shimming. A volume of interest with a thickness of 15 mm was placed on the centrum semiovale directly over the corpus callosum and parallel to the sphenoidal plane. After optimal water signal suppression with chemical shift selective techniques, MRS data were collected. The entire evaluation was completed within 7 minutes. Four specific voxels were selected from the bilateral parasagittal frontal and parietal gray matter and from the bilateral frontal and parietal white matter within the volume of interest. Spectra were generated by Fourier transformation from the data collected from these eight specific voxels within the volume of interest. After manual baseline correction (near zero) procedures, metabolite peaks were determined. Three dominant spectra (Cho at 3.21 ppm, Cr at 3.04 ppm, and NAA at 2.02 parts per million [ppm]) were analyzed. The Kolmogorov-Smirnov test was used to assess the compatibility of the metabolite ratios obtained from the eight specific voxels (bilateral frontal and parietal white matter and bilateral frontal and parietal parasagittal gray matter) with normal distribution. After it was confirmed that all metabolite ratios were normally distributed, the metabolic ratios (NAA/Cho, NAA/Cr, and Cho/Cr) of the children with psychomotor delay and of the controls were compared by use of Student s t-test. TABLE 1: Frontal Lobe Metabolite Ratios (Mean ± SD) Ratio Results Thirteen children had minor psychomotor delay, and seven children had moderate psychomotor delay. The NAA/Cho, NAA/Cr, and Cho/Cr ratios of the two groups of children for the frontal lobe voxels are shown in Table 1 and for the parietal lobe voxels in Table 2. No statistically significant differences between the psychomotor delay group and the control were found for any of the comparisons (Figs. 1 3). Discussion MRS, a noninvasive method that has gained wide clinical use and has been found beneficial in the assessment of neuronal function and metabolite discrepancies in the brain, was performed on children with psychomotor delay of unknown cause and who did not have abnormal MRI findings. To determine the changes in the brain metabolism of children with psychomotor delay, we compared the metabolite ratios obtained from to 15-year-old children with psychomotor delay and to 13-year-old children without psychomotor delay. When we compared the metabolite rates obtained from eight specific voxels, including the bilateral frontal lobe white matter and parasagittal gray matter and the bilateral parietal lobe white No. of Patients Voxel p NAA/Cho Right frontal white matter Right frontal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.23 Control ± ± 0.19 NAA/Cr Right frontal white matter Right frontal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.40 Control ± ± 0.20 Cho/Cr Right frontal white matter Right frontal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.26 Control ± ± 0.11 NAA/Cho Left frontal white matter Left frontal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.21 Control ± ± 0.15 NAA/Cr Left frontal white matter Left frontal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.33 Control ± ± 0.34 Cho/Cr Left frontal white matter Left frontal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.30 Control ± ± 0.22 Note NAA = N-acetylaspartate, Cho = choline, Cr = creatine. AJR:194, April
3 Koşucu et al. matter and parasagittal gray matter, no statistically significant difference was found between the two groups. Few studies reported in the literature have been conducted with children with psychomotor delay who underwent MRS. In a study by Filippi et al. [2], metabolite ratios obtained from the bilateral frontal and parietooccipital subcortical white matter of children younger than 2 years and older than 2 years with growth retardation and groups of age-matched healthy children were compared. Among the children younger than 2 years, there was no significant difference between the NAA/Cr and Cho/Cr ratios of children with growth retardation and those A of controls. Among the children older than 2 years, however, the NAA/Cr ratios were lower and the Cho/Cr ratios higher in children with growth retardation compared with the controls [2]. The investigators speculated that among the older children, the lower NAA/Cr ratios of children with psychomotor delay might have been associated with my- Fig. 1 Comparison of spectra obtained from right frontal lobe white matter. Insets show volume of interest in axial, sagittal, and coronal planes. ppm = parts per million. A, 6-year-old girl without psychomotor delay. MR spectroscopic readout shows metabolite ratios are N-acetylaspartate (NAA) to choline (Cho), 1.43; NAA to creatine (Cr), 1.88; and Cho/Cr, B, 6-year-old girl with mild psychomotor delay of unknown cause. MR spectroscopic readout shows metabolite ratios are NAA/Cho, 1.31; NAA/Cr, 1.95; and Cho/Cr, B A Fig. 2 Comparison of spectra obtained from left parietal lobe white matter. Insets show volume of interest in axial, sagittal, and coronal planes. ppm = parts per million. A, 6-year-old boy without psychomotor delay. MR spectroscopic readout shows metabolite ratios are N-acetylaspartate (NAA) to choline (Cho), 1.82; NAA to creatine (Cr), 2.00; and Cho/Cr, B, 6-year-old boy with psychomotor delay. MR spectroscopic readout shows metabolite ratios are NAA/Cho, 1.62; NAA/Cr, 2.11; and Cho/Cr, B 1112 AJR:194, April 2010
4 MR Spectroscopy of Psychomotor Delay elin damage, loss of normal myelin, synaptic intensity, or a reduction in the number of neurons. In the same report, the authors suggested that the increased Cho/Cr ratios in the group with growth retardation might have been associated with destruction of mature myelin or the inability of choline to enter into the macromolecules involved in myelin formation. Although Filippi et al. found no regional variations between the right and left hemispheres or the frontal and parietooccipital lobes, we, in agreement with other investigators [4, 13], did find regional variations in metabolite ratios. Specifically, the NAA/ Cho ratios in the right hemisphere were higher than the ratios in the left hemisphere, and the NAA/Cho ratios in the parietal lobe were higher than in the frontal lobe. Hashimoto et al. [4] used MRS to evaluate to 13-year-old children with psychomotor delay and age-matched healthy children, comparing the metabolite ratios obtained from the right frontoparietal lobe white matter. Those investigators found lower NAA/ Cr ratios in the psychomotor delay group but no significant difference in the Cho/Cr ratios of the two groups. In the same study, the NAA/Cho ratios of both groups were found to increase with age. This increase, however, was slower in the psychomotor delay group. The interpretation of these results was that brain development was delayed in patients with psychomotor delay; therefore, the NAA A Fig. 3 Comparison of spectra obtained from left frontal parasagittal gray matter. Insets show volume of interest in axial, sagittal, and coronal planes. ppm = parts per million. A, 6-year-old girl without psychomotor delay. MR spectroscopic readout shows metabolite ratios are N-acetylaspartate (NAA) to choline (Cho), 1.54; NAA to creatine, 1.73; and Cho/Cr, B, 6-year-old girl with psychomotor delay. MR spectroscopic readout shows metabolite ratios are NAA/Cho, 1.58; NAA/Cr, 1.25; and Cho/Cr, concentration was low compared with that of age-matched healthy children. Hashimoto et al. concluded that neuronal activity did not deteriorate but progressed slowly in children with psychomotor delay. Martin et al. [1] compared the NAA, myoinositol, Cr, and Cho peaks and NAA/Cr, myoinositol/cr, and Cho/Cr ratios in the frontoparietal white matter and deep gray matter of 48 children with psychomotor delay with the values in 23 healthy children and found no significant difference between the two groups in terms of metabolite levels and ratios. In agreement with the findings reported by Martin et al. [1], our findings show that the brain metabolite ratios of children with psychomotor delay of unknown cause were similar to the brain metabolite ratios of children without psychomotor delay. NAA is found mainly in the CNS, especially in the pyramidal neurons, dendrites, and axons, and is the most sensitive metabolite in the CNS. Therefore, it was identified as a neuronal determinant [2, 11, 14, 15]. The level of NAA decreases as the result of neuronal damage and loss or of demyelinization in clinical conditions, such as malignant tumors of the CNS, multiple sclerosis, mitochondrial disorders, AIDS, temporal lobe epilepsy, hypoxic injury, aging, Alzheimer s disease, and multiinfarct dementia [3, 9, 13, 16, 17]. Although NAA is present extensively in brain tissue, the functions of NAA in nerve tissue are not clearly understood. The NAA concentration in cerebral white and gray matter increases with age. It is impossible to explain the increase in NAA concentration with age by the number of neurons and neuronal proliferation because neuronal proliferation ends at birth. Martin et al. [1] suggested that the increase in NAA concentration with age may be associated with the development of synaptic terminals, dendritic arborization, and an increase in axonal diameter or myelination. However, when the theory that psychomotor delay is caused by a defect in the structure and function of dendritic spina [18, 19] is taken into account, NAA concentration in children with psychomotor delay is expected to be low. In contrast, NAA concentrations in children with psychomotor delay were not low in our study or the study by Martin et al. Choline is a structural component of all cell membranes and reflects cell turnover. Choline level increases during formation and resorption. Cho/Cr ratios are higher in infants than in adults. Because choline is present in the structure of myelin-associated macromolecules, increased myelination, which is a normal finding in the first months of life, leads to a decrease in Cho/Cr ratio. Therefore, although NAA/Cr ratio increases rapidly during the first postnatal month and through the first and second years, Cho/Cr ratio rapidly decreases through the first year and decreases slowly through the second year [2]. B AJR:194, April
5 Koşucu et al. TABLE 2: Parietal Lobe Metabolite Ratios (Mean ± SD) Ratio No. of Patients Voxel p NAA/Cho Right parietal white matter Right parietal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.44 Control ± ± 0.29 NAA/Cr Right parietal white matter Right parietal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.28 Control ± ± 0.24 Cho/Cr Despite the critical importance of the first year of life in the development of the nervous system, we did not include children with psychomotor delay who were younger than 3 years in our study because of difficulties in performing intelligence tests, the poor reliability of the results of these tests, and the need for sedation to perform reliable spectral analysis on children in this age group. Because the effects of medication on spectra are not known, sedatives were not administered to the children with psychomotor delay or to the controls in our study. There were limitations to our study. One of the limitations of MRS is that in the presence of tissues that cause great variation in magnetic sensitivity compared with brain tissue, such as bone, air, fat, and hemorrhage within or adjacent to the investigated tissue, artifacts caused by these structures cause difficulty in the acquisition of a homogeneous magnetic field. To obtain a homogeneous magnetic field in our study, we placed a volume of interest inside the centrum semiovale and left the bony structures, subarachnoid space, and ventricles out. Another limitation was that the signals produced in each voxel were not exclusively from the gray or white matter. Therefore, extreme Right parietal white matter Right parietal parasagittal gray matter Psychomotor delay ± ± 0.24 Control ± ± 0.15 > 0.05 NAA/Cho Left parietal white matter Left parietal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.38 Control ± ± 0.30 NAA/Cr Left parietal white matter Left parietal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.22 Control ± ± 0.23 Cho/Cr Left parietal white matter Left parietal parasagittal gray matter > 0.05 Psychomotor delay ± ± 0.20 Control ± ± 0.15 Note NAA = N-acetylaspartate, Cho = choline, Cr = creatine. caution was exercised in selection of specific voxels to include exclusively gray or white matter in an attempt to reduce the partial volume effect. Although there was no gray matter or CSF contamination in the specific voxels selected from the bilateral frontal and parietal lobe white matter, contamination caused by subcortical white matter and CSF from the subarachnoid space was evident in voxels selected from the bilateral frontal and parietal lobe parasagittal gray matter. As in previous studies, in our study a long TE (135 milliseconds) was used to assess NAA, Cho, and Cr metabolites. Spectral Cho, NAA, Cr, and lactate peaks usually form when a long TE is used. Fat tissue and macromolecules detected in a short TE are usually not observed in a long TE. Another limitation of MRS is the lack of precise measurement of the metabolite peak areas within the selected specific voxel due to the influences of magnetic field inhomogeneity. In addition, the peak areas of the metabolites can be influenced by the partial volume effect of various tissues within the volume of interest. Therefore, not the peak areas of the metabolites but the ratios of one peak area to another are more accurate determinants for verifying metabolite irregularities within tissues [13]. Therefore, in this study, rather than the metabolite amounts inside the voxel, metabolite ratios were compared with one another. Studies have been performed with singlevoxel technique, and limited brain volumes have been evaluated. Multivoxel MRS has a better signal-to-noise ratio. Use of MRS also makes it possible to obtain measurements from an extended region of the brain and from multiple voxels simultaneously. Among several studies in which children with psychomotor delay of unknown cause have been evaluated with MRS, the current study is the only one, to our knowledge, performed with multivoxel technique. We acquired metabolite ratio data from eight specific voxels simultaneously. Nevertheless, our metabolite ratio results did not exclude the possibility of differences in brain metabolite ratios in regions other than the brain volumes studied. We conclude that the brain metabolite ratios of children with psychomotor delay of unknown cause are similar to the metabolite ratios of age-matched children without psychomotor delay. Regional variations exist in the brain metabolite ratios of children with psychomotor delay of unknown cause, as they do in children without psychomotor delay. Further MRS studies with large numbers of subjects and of different brain regions consisting of deep gray matter nuclei are needed to determine the brain metabolite ratios and to detect whether metabolite differences are present in children with psychomotor delay of unknown cause. Other metabolites also should be measured in future MRS studies of these children. References 1. Martin E, Keller M, Ritter S, Largo RH, Thiel T, Loenneker T. Contribution of proton magnetic resonance spectroscopy to the evaluation of children with unexplained developmental delay. Pediatr Res 2005; 58: Filippi CG, Ulug AM, Deck MD, Zimmerman RD, Heier LA. Developmental delay in children: assessment with proton MR spectroscopy. Am J Neuroradiol 2002; 23: Angelie E, Bonmartin A, Boudraa A, Gonnaud PM, Mallet JJ, Sappey-Marinier D. Regional differences and metabolic changes in normal aging of human brain: proton MR spectroscopic imaging study. Am J Neuroradiol 2001; 22: Hashimoto T, Tayama M, Miyazaki M, et al. Developmental brain changes investigated with proton magnetic resonance spectroscopy. Dev Med Child Neurol 1995; 37: Pouwels PJ, Brockmann K, Kruse B, et al. Re AJR:194, April 2010
6 MR Spectroscopy of Psychomotor Delay gional age dependence of human brain metabo- ment with brain magnetic resonance imaging and ton MR spectroscopy. Am J Neuroradiol 2001; lites from infancy to adulthood as detected by proton magnetic resonance spectroscopy. J Clin 22: quantitative localized proton MRS. Pediatr Res Psychiatry 2003; 64: Vasconcelos MM. Mental retardation [in Portu- 1999; 46: Vythilingam M, Charles HC, Tupler LA, Blitch- guese]. J Pediatr (Rio J) 2004[2 suppl]; 80:S71 S82 6. Charles HC, Lazeyras F, Krishnan KR, et al. Pro- ington T, Kelly L, Krishnan KR. Focal and later- 15. Zimmerman RA, Wang ZJ. The value of proton ton spectroscopy of human brain: effects of age alized subcortical abnormalities in unipolar major MR spectroscopy in pediatric metabolic brain and sex. Prog Neuropsychopharmacol Biol Psychiatry 1994; 18: van der Voorn JP, Pouwels PJ, Hart AA, et al. Childhood white matter disorders: quantitative MR imaging and spectroscopy. Radiology 2006; 241: Verbruggen KT, Meiners LC, Sijens PE, et al. Magnetic resonance imaging and proton magnetic resonance spectroscopy of the brain in the diagnostic evaluation of developmental delay. Eur J Paediatr Neurol 2009; 13: Weiss U, Bacher R, Vonbank H, Kemler G, Ling A, Marksteiner J. Cognitive impairment: assess- depressive disorder: an automated multivoxel proton magnetic resonance spectroscopy study. Biol Psychiatry 2003; 54: Levitt JG, O Neill J, Blanton RE, et al. Proton magnetic resonance spectroscopic imaging of the brain in childhood autism. Biol Psychiatry 2003; 54: Alkan A, Sarac K, Kutlu R, et al. Proton MR spectroscopy features of normal appearing white matter in neurofibromatosis type 1. Magn Reson Imaging 2003; 21: Kadota T, Horinouchi T, Kuroda C. Development and aging of the cerebrum: assessment with pro- disease. Am J Neuroradiol 1997; 18: Scarabino T, Popolizo T, Bertolino A, Salvolini U. Proton magnetic resonance spectroscopy of the brain in pediatric patients. Eur J Radiol 1999; 30: Barkovich AJ, Baranski K, Vigneron D, et al. Proton MR spectroscopy for the evaluation of brain injury in asphyxiated, term neonates. Am J Neuroradiol 1999; 20: Carlisle HJ, Kennedy MB. Spine architecture and synaptic plasticity. Trends Neurosci 2005; 28: Purpura DP. Dendritic spine dysgenesis and mental retardation. Science 1974; 186: AJR:194, April
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