Indian Journal Psychiatry

Abstract

Context: Attention deficit hyperactivity disorder (ADHD) is a common neurodevelopmental disorder with wide repercussions. Since it is etiologically related to delayed maturation, neurological soft signs (NSS) could be a tool to assess this. Further the correlation of NSS with severity and type of ADHD and presence of Specific Learning Disability (SLD) would give further insight into it.
Aims: To study neurological soft signs and risk factors (type, mode of delivery, and milestones) in children with ADHD and to correlate NSS with type and severity of ADHD and with co-morbid Specific Learning Disability.
Settings and Design: The study was carried out in Child care services of a tertiary teaching urban hospital. It was a cross-sectional single interview study.
Materials and Methods : 52 consecutive children diagnosed as having ADHD were assessed for the presence of neurological soft signs using Revised Physical and Neurological Examination soft Signs scale (PANESS). The ADHD was rated by parents using ADHD parent rating scale.
Statistical Analysis: The data was analyzed using the chi-squared test and Pearson's co-relational analysis.
Results and Conclusions: Neurological soft signs are present in 84% of children. They are equally present in both the inattentive-hyperactive and impulsive-hyperactive types of ADHD. The presence of neurological soft signs in ADHD are independent of the presence of co-morbid SLD. Dysrrhythmias and overflow with gait were typically seen for impulsive-hyperactive type and higher severity of ADHD is related to more errors.

Keywords: Attention deficit hyperactivity disorder, neurological soft signs type and severity of soft signs, factors affecting neurological soft signs

Introduction

Attention deficit hyperactivity disorder (ADHD) is believed to be the most common childhood behavioral disorder in children, affecting around 5.2% of school-age population globally. ^[1] ADHD may affect certain areas of the brain that allow problem solving, planning ahead, understanding others' actions, and impulse control. ^[2],[3] ADHD is a neuro-developmental disorder characterized by inattention, hyperactivity/impulsivity, or combined, some symptoms of which must be present before the age of 7 years and impairment must be observable in at least two settings. It is two to four times more common in boys. Inattention probably reflects problems with the executive functions of memory. ^[4],[5] However, delay in the development (by 3 yrs), specially of the frontal and parietal cortex was believed to be responsible for the ability to control and focus thinking. In contrast, the motor cortex in the ADHD patients was seen to mature faster than normal, suggesting that both slower development of behavioral control and advanced motor development might be required for the fidgetiness or hyperactivity that characterizes ADHD. ^[6] 

Impulse control lags (of about 3-5 years when compared to normal children) because inhibitory impairments are thought to involve voluntary or executive inhibition of prepotent responses rather than impulsiveness that may be more motivationally controlled. ^[7]Mounting evidence further shows that these inhibitory deficits are not a function of other psychiatric disorders that may overlap with ADHD. ^[8] Regarding etiology, there's a growing consensus that the condition has neurobiological underpinnings. A general reduction of brain volume was found with the core ADHD features of inattention, hyperactivity, and impulsivity reflecting frontal lobe dysfunction but other brain regions particularly the cerebellum had also been implicated. ^[8],[9] 

Neurological Soft Signs (NSS) are non-normative performance on a neurological examination of motor and sensory functioning in the absence of a focal lesion. They are poor coordination, speed or accuracy of limb or axial movements, including those required to keep the balance, dysrhythmias, and overflow are often found during the clinical examination of young children. ^[10] They are studied in terms of timed and untimed motor movements. The most reliable of the timed motor movements are "speed of movements" and "dysrhythmias" in that order. ^{[8],[10],[11]} Of the individual soft signs, synkinesias (movement overflow; 40%) and mirror movements (30%) have the highest incidence at the younger ages. Overflow movements are those that are mirrored in other body parts (like limbs, head) and occur at the same time as in the part (s) intended to perform the movement. They are considered developmentally normal in young children (under 6) in whom they persist over time when cortical inhibitory functions fail to develop in order to stop the radiation of motoric impulses to body parts other than the target body part. They are indicators of delayed development of motor inhibition. ^[8],[9],[11] Dysrhythmia is an abnormality in an otherwise normal pattern of movements; it can be seen as an improper rhythm or timing of the movement. They and slowed speed of movement are findings connected with functional deficits in the cerebellum and basal ganglia. ^[12] NSS in young adults have been associated with a number of neuropsychiatric and behavioral disorders, such as psychosis, obsessive-compulsive disorder, and also in conditions of atypical development, like autism and learning disability and ADHD. ^{[13],[14],[15]} Our review of literature failed to find Indian studies on this subject. Thus, the study was planned with the aim of studying neurological soft signs and risk factors (type, mode of delivery, and milestones) in children with ADHD and the correlation of soft signs to type and severity of ADHD and with the co-morbidity of specific learning disability.

Materials and Methods

School Mental Health Services and Centre for Learning Disability in a tertiary care teaching Municipal Hospital was the site of study. Permission was taken from the institutional review board. A cross-sectional interview was conducted in 52 consecutive children diagnosed as having ADHD to assess severity of ADHD and neurological soft signs. The inclusion criteria were children between 6 and 16 years and diagnosed to have ADHD by the psychiatrist based on the DSM IV criteria. Children with mental retardation, seizure disorder, and other physical ailments with obvious neuropathology were excluded. All the children diagnosed as having ADHD and fulfilling above criterion were interviewed after obtaining due informed consent from the parents and assent from children.

Assessments

The semi-structured proforma contained demographics, educational and socioeconomic status, family history, birth and development history. The children were rated using ADHD parent rating scale and examined for neurological soft signs using PANESS (physical and neurological examination for soft signs).The ADHD parent Rating Scale is a scale used to assess severity of ADHD in children. It was originally devised by G. P. DuPaul and can be used by parents and teachers. Cronbach's alpha for total score is 0.94, inattention-hyperactivity 0.93 and for impulsive hyperactivity 0.90. Test-retest reliability for total score is 0.94. It consists of 14 items which are rated on a Likert scale from 0 (not at all) to 3 (very much). It has two sub-factors, one of impulsive-hyperactive and another of inattentive-hyperactive type. There is a total score which ranges from 0 to 42. For purpose of defining severity, scores less than 14 were designated as mild and more than 28 designated as severe, those between the two were of moderate intensity.

PANESS is a Revised Physical and Neurological Examination for soft Signs scale by Martha Denckla . It is used for physical and neurological soft signs. It can be used for children and adolescents. It is an observational scale having 21 questions covering gait, stance, laterality, quality of rapid movements, impersistence score, involuntary movement score, repetitive speed of movement score, and sequenced speed of movement score, asymmetrical movement score. It assesses in terms of laterality, timed and untimed motor movements. It has been found to have adequate test retest reliability, inter-rater reliability, and internal consistency. The PANESS is particularly useful for assessment of motor speed in children because it is brief, minimizes the need for equipment, provides lateralized data, and is applicable to children as young as 5 years. ^[16] 

Scoring

For the gait tasks, the examiner scored the number of errors in a sample of 10 steps, and recorded the presence of feet to- hand overflow (i.e. extension of the hand at the wrist during heel walking). For balance tasks, the number of hops (maximum of 50) and seconds standing (maximum of 30 for each foot) was recorded. For repetitive timed movements, the time to complete 20 movements was recorded using a stopwatch, as well as the presence of overflow (proximal, oro-facial, and mirror movements) and dysrhythmia. Dysrhythmia was also recorded during hopping. For the motor persistence task, the time that the child could maintain closed eyes was recorded (maximum of 20 s for each stance). The examiner also recorded any abnormal movements (i.e. choreiform movements and limb tremor) seen during the examination. The times for repetitive and patterned movements were converted to z-scores based on published normative data. For measures of gait, balance, motor persistence, overflow, dysrhythmia and impersistance, ordinal scores (0, 1, and 2) were given, with higher scores indicating increasing abnormal performance. Ordinal scores were summed across the right and left sides of the body for all measures to create summary scores for the following categories: (1) Gaits - error scores for heel, toe, sides of feet, and tandem gaits; (2) Balance - error scores for one-footed hops and stands; (3) Speed of repetitive timed movements - z-scores were summed; and (4) Speed of patterned timed movements - z-scores were summed, (5) Dysrhythmia - on timed movements; (6) Overflow - on gait and timed movements. For those tests where no standard scores are defined, the presence of the soft sign above the age of 7 years was taken as abnormal.^[14],[16] 

Statistical analysis

The data was pooled and analyzed using SPSS version 16. The chi-square test was applied wherever applicable.

Results

Studied in three parts

I. Demography

II. Risk factors

III. Neurological soft signs

Demographic details

The mean age of the children was 10.23+/_2.45 and the range was 6-15 years. Most of the children in our study were male (84%) and from nuclear family (75%). Also 50% of them were from middle, 48.1% from upper, and only 1.9% from lower class (according to modified Kuppuswami scale). ^[17] However this may be a reflection of utilization of services by middle and higher class. Also most fell into the category of moderate (51.9%) and severe (46.2%) types of ADHD, remaining 1.9% were mild. Similarly, 65.4% had ADHD alone and 34.6% had ADHD with co-morbid Specific Learning Disability. None of the subjects had significant psychiatric or medical history. Three had a history of ADHD in either first or second degree relatives, while one mother had bipolar illness and another had hypothyroidism.

Assessment of risk factors

Pre term delivery

Most (90.4%) of the ADHD were born full term.

Type of delivery

67.3% had a normal delivery whilst others had a section, forceps or vacuum extraction.

Developmental milestones distribution

71% of ADHD children from our study had developmental delay; out of which 23% were found to be delayed in motor, 33% in language, and 15% in social milestones.

Neurological soft signs

Studied considering following factors.

1. Co-morbid Specific Learning Disability

2. NSS distribution

3. Age

4. ADHD type vs Soft Signs

Untimed motor movements

Timed motor movements

5. ADHD severity vs Soft Signs

Untimed motor movements

Timed motor movements

Co-morbid specific learning disability

The soft signs did not differ between the two groups, children with ADHD and those with ADHD and Specific Learning Disability. Hence further analysis was as a single group.

NSS distribution

Overall 84% of the children from our study had NSS of which 87% had soft signs on untimed movements while 82% had on timed. Further on timed movements 85% showed soft signs on repetitive movements and 80% on patterned movements. Most of the untimed movements were observed on gait and balance movements (100%), overflow movements with gait (93%), involuntary movements (88%), impersistence movements (67%).On timed they were observed for dysrhythmia (96%) and overflow (repetitive-87% and patterned-80%) and Speed of movements (repeative-72% and paterened-63%).

Age

In our study 84% children had NSS. In children with both the types of ADHD, NSS had a significant statistical correlation with age. The severity of symptoms decreased as age advances.

ADHD type vs soft signs

On untimed movements most of these errors were statistically significant in both types of ADHD [Table 1].

Table 1: Comparison between ADHD type and untimed soft signs nonparametric correlations between PR inattentive hyperactivity sum total and PR impulsivity hyperactivity sum total vs various PANESS components in diagnosed ADHD Click here to view

Now at this point before going on to timed motor movements, it would be worth telling that six of the ADHD children who were of age 7 years or less and whose score on ADHD Parent rating scale was above 35 (i.e. severe) were unable to perform the timed motor movements of PANESS scale due to hyperactivity. Hence, data is not available for six of them.

For impulsive hyperactive type soft signs were mostly significant for timed movements were dysrhythmia errors [Table 2]. Overall, the NSS timed and untimed, that are statistically significant in both impulsive and inattentive type of ADHD, were gait and balance error, dysrhythmia error, impersistance score, involuntary movement score, and total overflow with gait. The NSS statistically seen only in inattentive hyperactive type of ADHD are overflow with repetitive movements (right left as well as excess for age) and total overflow errors.

Table 2: Comparison between ADHD type and timed soft signs nonparametric correlations between PR inattentive hyperactivity sum total and PR impulsivity hyperactivity sum total vs various PANESS components in diagnosed ADHD Click here to view

Adhd severity vs soft signs

Most of the statistically significant differences between moderate and severe types of ADHD were found on untimed motor movements (gait and balance, involuntary movements) [Table 3].

Table 3: Comparison between ADHD severity and untimed soft signs nonparametric correlations between severities of ADHD vs various PANESS components in diagnosed ADHD Click here to view

On timed movements, the severe form of ADHD had significant errors on overflow with patterned and timed movements and repetitive speed of movement. [Table 4] Overall, NSS both timed and untimed increases with severity of ADHD.

Table 4: Comparison between ADHD severity and timed soft signs nonparametric correlations between severities of ADHD vs various PANESS components in diagnosed ADHD Click here to view

Discussion

Demography

ADHD is known to be more in males. ^[18],[19] The increased prevalence of higher socio-economic status and co-morbidity of dyslexia may be a representation of utilization of our services by the affluent parents visiting our center which is a certifying authority for specific learning disorders. A widely variable overlap ranging from 10% to 92% has been reported in the literature between ADHD and Specific Learning Disability ^[20],[21] whereas, between 19% and 26% of children with ADHD are likely to have any single type of learning disability. ^[9] Nuclear families are also becoming a norm in Mumbai. A family history of ADHD, substance abuse, and personality disorder is commonly seen in children with ADHD.

Assessment of risk factors

Prematurity

Studies have reported higher prematurity in children with ADHD. ^[20],[22] However, we did not see this.

Type of delivery

Nearly one third of our children had a section, vacuum or forceps assisted delivery. Caesarean section is known to be a risk factor for ADHD ^[23] 

Milestones

Delay in milestones is in consistence with the earlier studies where the incidence was 52% for motor; 33-35% for language development and 15.4% were delayed in social milestones . ^[9] In fact, speech delay with inattention and soft signs are known to be early predictors of ADHD. ^[24] 

Neurological soft signs

With co-morbid specific learning disability

When ADHD and SLD co-occur, it has been seen that the soft signs are more related to ADHD than with Specific Learning Disability. This is in keeping with other studies where motor signs were more in ADHD as compared to controls or those with Specific Learning Disability. ^[11] 

NSS distribution

NSS are known to be able to discriminate between non-clinical and clinical groups of children. Children with hyperactivity had significantly higher scores of overflow movements when compared to other children with behavioral problems. ^[25] It was also found that children with ADHD had more soft signs related to motor coordination and motor overflow movements when compared with control children including those with purely Specific Learning Disability. Children with problems such as hyperactivity, impulsivity, reading difficulties, or school underachievement were found to differ significantly with respect to soft signs. ^[11] Overflow movements are known to be more in children with ADHD and reflect immaturity of cortical functions. Overflow movements are indicators of delayed development of motor inhibition. ^[8],[11] The deficit in cortical inhibitory functions is a cardinal neurophysiologic feature of ADHD. ^[26] Children with hyperactivity had significantly higher scores of overflow movements when compared to other children with behavioral problems. ^[25] Dysrhythmic movements are findings connected with functional deficits in the cerebellum and basal ganglia. ^[12] Motor proficiency, as seen in speed, rhythm, and absence of overflow, has differentiated non-learning disabled hyperactive boys from matched controls. ^[27] In fact, speed, rhythm, and overflow could help in classifying 89% of the boys as those with "hyperactive" versus "normal" behavioral histories.^[27] Speed of movement, overflow with timed movements, asymmetry of error, dysrhythmia (quality of movement), and overflow with gaits are seen to be the important factors in differentiating ADHD with or without LD from their non disabled counterparts. ^[11] Thus, quality and speed of movement is affected in children with ADHD.

Age

The age at which NSS are expected to be absent or pathological has not been established, but studies says by age 7, many of the skills assessed by the PANESS have reached "adult" level in typically developing children. ^[28] If present beyond they indicate neuro-maturational delay. However, different studies have different opinion over this. We decided to go by this age (7 yrs) for few untimed movements whose norms are not available. In our study, 84% children had NSS. Thus, there was a high incidence of maturational delay. This delay has been reported in many earlier studies. ^{[14],[25],[29],[30]} Similarly decreasing incidence of soft signs with age has also been reported. ^[31] It is believed that this decrease with age is due to the integration of higher order processes, such as attention, with lower-level neuromotor inhibitory mechanism. ^[32] 

Type of ADHD

Very few studies have researched on this aspect of ADHD. In a study, children with inattentive type of ADHD had significantly poorer fine motor skill, while children with combined ADHD were found to experience significantly greater problems with gross motor skill. ^[23] Untimed movement errors were present in both types. This is in keeping with other studies ^[24] Children with impulsivity had more of dysrhythmias which are indicative of cerebellar pathology. The inattentive sub-type had significant overflow which is more indicative of delayed motor inhibition.

Severity of ADHD

We could not find studies which have researched on severity of ADHD and soft signs. Significant scores are seen more when the severity of the ADHD is higher. Both timed and untimed errors occur. This probably reflects an increase in risk factors predisposing to ADHD and therefore also soft signs. When compared to normal, children with ADHD significantly differ with respect to soft signs and there is certain correlation of NSS with neurodevelopmental disorders like ADHD. ^{[24],[28],[29]} 

Conclusions

Demographic

• Most of the ADHD were born full term.
• None of the subjects had significant past psychiatric or medical history.

Neurological soft signs

• Present in all ages with ADHD and decreases with age.
• Dysrhythmias and overflows were maximum.
• Independent of the presence of co-morbid SLD.
• Almost equally present on timed and untimed movements.

Type

• Children with both the types of ADHD had NSS.
• Impulsive-hyperactive children had more problems on untimed movement.

Severity of ADHD

• Children with severe ADHD had more problems on timed movements especially for repetitive tests.

Limitations

1. The present study was limited with a relatively small sample size, which precluded comparisons according to sex and age of children.
2. The normative data for the PANESS was not of Indian children.

Implications

The assessment needed minimal training and was neither time nor labor intensive. Apart from a stopwatch, no additional equipment is needed. From a practical aspect therefore, the assessment of soft signs with this is quick and easy to perform. However, how would we interpret scores in the clinical setting and still remains an area for further research.

Could severity of neurological soft signs in ADHD, predict future problems in fine motor performances in the Indian setting is also a question for further research.

 

References

1.	Kaplan and Sadock's. Attention Deficit Disorders. In: Sadock BJ, Sadock VA, editors. Comprehensive Textbook of Psychiatry, 9 th ed. Philadelphia: Wolters Kulwer; 2009. p. 3560-1.
2.	Ramsay JR. Cognitive Behavioural Therapy for Adult ADHD. Routledge 2007. Available from: http://en.wikipedia.org/wiki/Attention-deficit_hyperactivity_disorder [Last accessed on 2010 May 30].
3.	American Academy of Child Adolescent Psychiatry. ADHD - A Guide for Families 2009. Available from: http://www.aacap.org/cs/adhd_a_guide_for_families/what_is_adhd [Last accessed on 2009 Aug, 20].
4.	Barkley RA, Cunningham CE. The effects of methylphenidate on the mother.child interactions of hyperactive children. Arch Gen Psychiatry 1979;36:201-8. (Pubmed).
5.	Sergeant J. DSM-III attentional deficit disorder to functional defects. In: Bloomingdale L, Sergeant J, editors. Attention deficit disorder: Criteria, cognition, and intervention. New York: Pergamon; 1988.p. 183-98.
6.	Brain Matures a Few Years Late in ADHD, But Follows Normal Pattern. NIMH Press Release, November 12, 2007. Available from http://www.nimh.nih.gov/science-news/2007/brain-matures-a-few-years-late.in.adhd.but.followsnormal- pattern.shtml [Last accessed on 2010 Apr 22].
7.	Nigg JT. Inhibition/disinhibition in developmental psychopathology. Views from cognitive and personality psychology and a working inhibition taxonomy. Psychol Bul 2000;126:220-46. (Pubmed).
8.	Krain AL, Castellanos FX. Brain development and ADHD. Clin Psychol Rev 2006;26:433-44.
9.	Barkley RA. Attention-Deficit/Hyperactivity Disorder: Nature, Course, Outcomes, and Co morbidity 2006. Available from: http://www.continuingedcourses.net/active/courses/course003.php [Last accessed on 2010 Apr 25].
10.	Martins I, Lauterbach M, Slade P, Luis H, De Rouen T, Martin M, et al. A longitudinal study of neurological soft signs from late childhood into early adulthood. Dev Med Child Neurol 2008;50:602-7.
11.	Denckla MB, Rudle RG, Chapman C, Krieger J. Motor proficiency in dyslexic children with and without attentional disorders. Arch Neurol 1985;42:228-31.
12.	Kandel ER. Principles of Neural Science. Turk J Pediatr 2007;49:263-9.
13.	Mandelbaum DE, Stevens M, Rosenberg E, Wiznitzer M, Steinschneider M, Filipek P, et al. Sensorimotor performance in school-age children with autism, developmental language disorder, or low IQ. Dev Med Child Neurol 2006;48:33-9.
14.	Dickstein DP, Garvey M, Pradella AG, Greenstein DK, Sharp WS, Castellanos FX, et al. Neurologic examination abnormalities in children with bipolar disorder or attention deficit/hyperactivity disorder. Biol Psychiatry 2005;58:517-24.
15.	Shafer SQ, Stokman CJ, Shaffer D, Ng SK, O'Connor PA, Schonfeld IS. Ten-year consistency in neurological test performance of children without focal neurological deficit. Dev Med Child Neurol 1986;28:417-27.
16.	Denckla MB. Revised Physical and Neurological Examination for Subtle Signs. Psychopharmacol Bull 1985;21:773-800.
17.	Mishra D, Singh HP. Kuppuswamy socioeconomic status scale-A revision. Indian J Pediatr 2003;70:273-4.
18.	Du Paul GJ, Power TJ, Anastopoulos AD ADHD rating scale-IV: checklists, norms, and clinical interpretation. New York: The Guildford Press; 1998.
19.	Breton JJ, Bergeron L, Valla JP, Berthiaume C, Gaudet N, Lambert J, et al. Quebec Child Mental Health Survey: Prevalence of DSM-III-R Mental Health Disorders. J Child Psychol Psychiatry 1999;40:375-84.
20.	Carte ET, Nigg JT, Hinshaw SP. Neuropsychological functioning, motor speed, and language processing in boys with and without ADHD. J Abnorm Child Psychol 1996;24:481-98.
21.	Semrud-Clikeman M, Biederman J, Sprich-Buckminster S, Lehman BK, Faraone SV, Norman D. Comorbidity between ADDH and learning disability: A review and report in a clinically referred sample. J Am Acad Child Adolesc Psychiatry 1992;31:439-48.
22.	Mostofsky SH, Newschaffer CJ, Denckla MB. Overflow movements predict impaired response inhibition in children with ADHD Perceptual and Motor Skills. Percept Mot Skills 2003;97:1315-31.
23.	Valdimarsdottir M, Hrafnsdottir AH, Magnusson P, Gudmundsson OO. The frequency of some factors in pregnancy and delivery for Icelandic children with ADHD. Laeknabladid 2006;92:609-14.
24.	Piek JP, Pitcher TM, Hay DA. Motor coordination and kinaesthesis in boys with attention deficit-hyperactivity disorder. Dev Med Child Neurol 1999;41:159-65.
25.	Szatmari P, Taylor DC. Overflow movements and behavior problems: Scoring and using a modification of Fogs' test. Dev Med Child Neurol 1984;26:297-310.
26.	Fog E, Fog M. Cerebral inhibition examined by associated movements. In: Bax M, Mac Keith R, editors. Minimal Cerebral Dysfunction. Clinics in Developmental Medicine No.10. London: SIMP with Heinemann Medical; 1963.
27.	Denckla M, Rudel RG. Anomalies of motor development in hyperactive boys. Ann Neurol 2004;3:231-3.
28.	Gidley Larson JC, Mostofsky SH, Goldberg MC, Cutting LE, Denckla MB, Mahone EM, et al. Effects of Gender and Age on Motor Exam in Typically Developing Children. Dev Neuropsychol 2007;32:543-62.
29.	Vitiello B, Stoff D, Atkins M, Mahoney A. Soft neurological signs and impulsivity in children. J Dev Behav Pediatr 1990;11:112-5.
30.	Gottesman RL, Hankin D, Levinson W, Beck P. Neurodevelopmental functioning of good and poor readers in urban schools. J Dev Behav Pediatr 1984;5:109-15.
31.	Remo HL, Jon AC. Neuromotor development from 5 to 18 years: associated movements Dev Med Child Neurol 2001;43:444-53.
32.	Lazarus JA, Todor JI. The role of attention in the regulation of associated movement in children. Dev Med Child Neurol 1991;33:32-9.

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http://www.indianjpsychiatry.org/article.asp?issn=0019-5545;year=2012;volume=54;issue=2;spage=159;epage=165;aulast=Patankar