Small-for-gestational-age newborn infant: repercussion on fine motor skills

Abstracts

OBJETIVO: Comparar as habilidades motoras finas de lactentes nascidos a termo pequenos para a idade gestacional (PIG) com as habilidades dos nascidos adequados para a idade gestacional (AIG) no terceiro mês de vida. MÉTODOS: Realizou-se um estudo observacional de corte transversal. Avaliaram-se 67 lactentes (21 PIG e 46 AIG) no terceiro mês de vida. Portadores de síndromes genéticas, malformações congênitas, infecções congênitas e aqueles que necessitaram de unidade de terapia intensiva neonatal foram excluídos. As Escalas Bayley II de Desenvolvimento Infantil foram utilizadas, com ênfase nos itens que avaliam as habilidades motoras finas. RESULTADOS: Não se observaram diferenças entre os grupos na escala motora (p=0,21) e mental (p=0,45) no terceiro mês de vida. No item "Alcança o Aro Suspenso", houve diferença significativa (teste Exato de Fisher; p=0,02), demonstrando maior frequência de execução para o grupo PIG no terceiro mês de vida. CONCLUSÕES: Supõe-se que a diferença encontrada no item "Alcança o Aro Suspenso" possa ser atribuída à grande ocorrência de movimentos dos braços observada no grupo PIG e não a uma condição melhor de desenvolvimento desse grupo.

retardo do crescimento fetal; comportamento do lactente; desempenho psicomotor; destreza motora

ORIGINAL ARTICLE

Amabile Vessoni Arias^I; Vanda Maria G. Gonçalves^II; Denise Campos^I; Denise Castilho C. Santos^III; Maura Mikie F. Goto^I; Thatiane Moura C.-Zanelli^IV

^IDoutora em Ciências Médicas pela Faculdade de Ciências Médicas da Unicamp, Campinas, SP, Brasil

^IILivre-docente pela Faculdade de Ciências Médicas da Unicamp; Professora Associada do Departamento de Neurologia e do Ciped da Faculdade de Ciências Médicas da Unicamp, Campinas, SP, Brasil

^IIIDoutora em Ciências Médicas pela Faculdade de Ciências Médicas da Unicamp; Professora de Fisioterapia da Faculdade de Ciências da Saúde da Unimep, Piracicaba, SP, Brasil

^IVMestre em Ciências Médicas pela Faculdade de Ciências Médicas da Unicamp, Campinas, SP, Brasil

Endereço para correspondência

ABSTRACT

OBJECTIVE: To compare the fine motor skills of full-term small-for-gestational-age (SGA) and appropriate-for-gestational-age (AGA) infants in the third month of life.

METHODS: This observational cross-sectional study enrolled 67 infants (21 SGA and 46 AGA) in the third month of life. Infants presenting genetic syndromes, congenital malformations, congenital infections and those who needed neonatal intensive care were excluded. The Bayley Scales of Infant Development-II were used, with emphasis on items that evaluate the fine motor skills.

RESULTS: No differences were observed between groups for motor (p=0.21) and mental (p=0.45) scales in the third month. There was a significant difference between the groups on the item "Reaches for Suspended Ring" (Fisher's exact test; p-value=0.02): a higher percentage of SGA infants accomplished this item in the third month of life.

CONCLUSIONS: We hypothesize that the difference found in the item "Reaches for Suspended Ring" could be attributed to an increased frequency of arm movements observed in SGA infants and not to a better neurodevelopment of this group.

Key-words: fetal growth retardation; infant behavior; psychomotor performance; motor skills.

RESUMEN

OBJETIVO: Comparar las habilidades motoras finas de lactantes nacidos a término pequeños para la edad gestacional (PEG) con adecuados para la edad gestacional (AEG) en el 3^er mes de vida.

MÉTODOS: Se realizó un estudio observacional de corte transversal. Se evaluaron a 67 lactantes (21 PEG y 46 AEG) en el 3^er mes de vida. Síndromes genéticos, malformaciones congénitas, infecciones congénitas y aquellos que necesitaron de unidad de terapia intensiva neonatal fueron excluidos. Las Escalas Bayley II y de Desarrollo Infantil fueron utilizadas, con énfasis en los ítems que evalúan las habilidades motoras finas.

RESULTADOS: No se observaron diferencias entre los grupos en la escala motora (p=0,21) y mental (p=0,45) en el 3^er mes de vida. En el ítem "alcanza aro suspendido" hubo diferencia significativa (p=0,02; prueba Exacta de Fisher), demostrando mayor frecuencia de ejecución para el grupo PEG en el 3^er mes de vida.

CONCLUSIONES: Se supone que la diferencia encontrada en el ítem "alcanza el aro suspendido" pueda ser atribuida a la gran ocurrencia de movimientos de los brazos observada en el grupo PEG y no a una condición mejor de desarrollo en este grupo.

Palabras-clave: retraso del crecimiento fetal, comportamiento del lactante, desempeño psicomotor, destreza motora.

Introduction

the development of small-for-gestational-age (SGA) newborns has continually been target of research because it is considered a model of malnutrition at early age. Since the 1960s and 70s, the attention of researchers has been caught by the fact that SGA infants suffer from a certain degree of malnutrition, a condition that could permanently limit their intellectual capacity in a technologically advanced world⁽¹⁾. Intrauterine malnutrition, which is defined as birth weight below the 10th percentile of the birthweight-for-gestational-age reference curve, affects 23.8%, or approximately 30 million newborns per year. Overall, nearly 75% of all affected newborns are born in Asia, mainly in South-central Asia, 20% in Africa, and approximately 5% in Latin America. Although some of them are healthy, in most developing countries a large proportion of newborns suffer from some degree of intrauterine malnutrition⁽²⁾.

While the neurodevelopment of preterm SGA and appropriate-for-gestational-age (AGA) children has been extensively studied during the past decades, much less attention has been paid to term SGA children. Although there is some evidences that SGA term infants may be associated with an increased risk of cerebral palsy, this affects very few children, being more common the neurodevelopmental deficits⁽³⁾. Some authors have reported motor delay at some stages in infancy^(4-10), a higher prevalence of motor problems related to academic achievement in adolescents, and professional attainment in adults⁽¹¹⁾; however, other studies do not support these findings^{(12, 13)}.

Early identification of children with motor impairments is important in order to provide support and intervention for the child (and parents) as early as possible. Optimal treatment for motor problems may reduce academic and psychosocial problems⁽¹⁴⁾. Very little research has attempted to assess specifically fine motor skills in full-term SGA infants. They consist in an important ability in early development and can provide a warning to the delayed motor development. For instance, object exploration plays a central role in the early development of perception, action, and memory. By seeing and touching objects, by bringing them to the mouth, and by manipulating them, infants can learn about their physical properties, remember their specific characteristics, and use this newly acquired knowledge to plan future actions⁽¹⁵⁾. The importance of these skills is reported to the older children too. Children spend 31 to 60% of their school day performing handwriting and other fine motor tasks, and difficulty in this area can interfere with their academic achievement. Fine motor control, bilateral and visual-motor integration, motor planning, in-hand manipulation, proprioception, visual perception, sustained attention, and sensory awareness of the fingers are some of the component skills that may interfere with future performance of handwriting⁽¹⁶⁾. The first months of life have been seen as an important period for early detection of neuromotor developmental disorders. Some studies showed that the observation of generalized spontaneous movements, between two and four months postterm, has predictive power for the development of coordination problems and fine manipulative disability in later childhood^{(17, 18)}.

Taking to account that there are few studies related to SGA infants in developing countries, especially studies with regard to fine motor skill, that identifying infants with less obvious delays can be a challenge, because such disabilities only become obvious gradually over time⁽¹⁹⁾; and that identifying infants at risk during the first trimester of life provides the opportunity of early referral for interventional services⁽²⁰⁾, this study was designed to increase knowledge about the fine motor skill of an understudied group, with possible clinical perspective of early detection. The purpose of this study was to compare the fine motor skills between full-term SGA with AGA infants in the 3^rd month of life.

Methods

The research design consisted of an observational cross-sectional study of two cohorts of full-term infants, one of full-term SGA group and another of control AGA group. This project was approved by the Research Ethics Committee at the Faculty of Medical Sciences of the University of Campinas (Unicamp), according to the provisions and principles of resolution 196/96 of the National Health Council.

A neonatologist selected 125 neonates delivered at Neonatology Service of the Center of Integral Attention to the Woman's Health (Caism/Unicamp), São Paulo, Brazil, between May 2000 and July 2003. When a SGA neonate was chosen, the following two AGA neonates were selected. The subjects were selected using the following criteria: 1) subjects living in the metropolitan area of Campinas; 2) newborns of single-fetus pregnancies, 3) considered to be in good health, allowing they go home within two days of birth; 4) gestational age categorized as full-term (37-41 weeks)⁽²¹⁾ by the Capurro method; 5) expected birth weight categorized by the Battaglia and Lubchenco method⁽²²⁾; birth weight less than 10th percentile for the SGA group and between 10th and 90th percentiles for the AGA group; and 6) parents were willing to sign the consent forms. Neonates with genetic syndromes, multiple congenital malformations and congenital infections (syphilis, toxoplasmosis, rubella, cytomegalovirus and herpes) were excluded.

From the initial selected sample (125), 95 (33 PIG e 62 AIG) infants returned for at least one assessment during the first year, at 3^rd month 67 full term infants (21 SGA and 46 AGA) were assessed and integrated the studied group. The number of participants selected for the study was signed during the three years of project development, considering the period of selection and assessment of subjects consistent with the deadlines for commencement and completion of the project and consistent with the demand of hospitalizations for pregnancy resolution in CAISM/UNICAMP. The number of participants was composed of all subjects who met the criteria for inclusion in the current period of the project, who joined the study and were evaluated at 3 months of life.

Accurate tools for measuring development are central in identification, classification and diagnosis of neurodevelopmental delays. Among these, the Bayley Scales of Infant Development (BSID-II) are commonly used in scientific studies and are considered gold standard for assessing children's development⁽²³⁾. In this study, the instrument used for examining the developmental functioning of infants was the BSID-II, which consists of three scales - mental, motor and behavior rating scales⁽²⁴⁾. Considering that BSID-II allows to study skill related items, in order to understand specific functional abilities of infants, the items "manipulates ring", "reaches for suspended ring", "grasps suspended ring" and "carries ring to mouth" were selected to investigate the fine motor skills in the 3^rd month.

The infant's score for each item was registered in the motor and mental scale record forms. The BSID-II motor and mental scale scores were obtained from the number of tests undergone by the infant. By summing the number of tests equivalent to earlier ages, the raw score (RS) was obtained. The RS score was converted into standardized points, obtaining an index score (IS) with a mean of 100 and a standard deviation of 15. Based on their IS, infants can be classified as having accelerated performance (IS > 115), within normal performance limits (IS 85 to 114), mildly delayed performance (IS 70 to 84) or significantly delayed performance (IS < 69). The motor and mental IS indicate the performance of infant at a given age on BSID-II. To further aid interpretation of infant's performance, it may also be examined the infant's performance on an item or set of items in isolation to gain more insight into that performance and it could allow more precise research⁽²⁴⁾.

All infants were assessed at the Laboratory for Study of Child Development of Unicamp. The testing room was quiet, well lit, well ventilated, without bright or colorful pictures, and free of distractions. All infants were assessed in the presence of their mothers during intervals between feeds, when infants were alert and cooperative. The infants were evaluated at three months of age and the range permitted was seven days before or after the respective age of assessment⁽²⁴⁾.

Assessments were performed by an examiner and simultaneously monitored by two observers who were unaware of the classification of the neonate's group. The testers comprised a pediatric neurologist, a pediatrician and a physical therapist, members of the Interdisciplinary Group for Infant Development Evaluation (GIADI). Prior to the assessments, the testers participated in the reliability training for the BSID-II, consisting of a didactic session of approximately 20 hours; each tester observed 12 videotaped tests and scored independently. The intraclass correlation coefficient was 0.95 (p<0.001), with a 95% confidence interval of 0.88-0.98.

All the materials necessary for testing the infants were included in the test kit, the material used was a red ring with string. Each item contains explicit instructions with all of the information necessary to administer that item properly. The study items are briefly described below:

"Manipulates Ring": place the ring in the child's hand. Observe the child to see if they shake the ring, move it into his field of vision, tilt it back and forth in one hand, or use both hands to finger it. Give credit if the child exhibits any manipulation of the ring beyond mere grasping; this includes ring mouthing.

"Reaches for Suspended Ring": suspend the ring by its string so that the lower edge of the ring is at the child's midline and approximately 20 to 25 centimeters directly above their eyes. Move the ring slightly to attract the child's attention; then hold it in stationary position. If the child does not reach for the ring, place the ring in one of the child's hands and allow them to manipulate it for a short time to generate interest in it; afterwards, repeat this item. Give credit if the child purposely moves their arm(s) in the ring direction while looking at the ring.

"Grasps Suspended Ring": suspend the ring by its string so that the lower edge of the ring is at the child's midline and approximately 20 to 25 centimeters directly above their eyes. Move the ring slightly to attract the child's attention; then hold it in stationary position. If the child does not reach for the ring, place the ring in the child's hand and allow them to manipulate it for a short time to generate interest in it; then repeat this item. Give credit if the child uses one or both hands to grasp the ring for at least two seconds.

"Carries Ring to Mouth": place the ring in the child's hand and observe what he does with it during this free-play period. Give credit if the child purposely carries the ring to their mouth.

Statistical analyses were performed using the Statistical Package for Social Sciences for Personal Computer (SPSS/PC 11.0). The probability level adopted for rejection of the null hypothesis was p<0.05. The Mann-Whitney test was used to investigated birthweight, Apgar index, gestational age and to determine the relation between continuous variables (mental and motor IS). The relation between categorical variables (fine motor skills items, gender) was investigated using the Chi-Square or Fisher's exact test.

Results

A total of 67 infants were studied. The sample for the observational cross-sectional study consisted of 21 SGA and 46 AGA infants in the 3^rd month of life.

Table 1 shows the newborn characteristics of the SGA and AGA groups (birthweight, Apgar scores in the 1^st and 5^th min, gestational age). As expected, groups were different regarding birthweight. Regarding to gender, no differences were observed between SGA and AGA groups (female: 52.4% in the SGA group and 56.5% in the AGA group; p=0,751).

Table 2 shows the distribution of socio-demographic profile of the family. The SGA and AGA groups had homogeneous distribution of the variables, except for maternal education and occupation, with a greater frequency of SGA group mothers presenting fewer than 8 years of study and not working outside home.

Figure 1 and Figure 2 show distribution motor and mental IS in the 3^rd month. Regarding to mental IS, the SGA and AGA groups were within the normal range (100±15). Contrasting to mental IS, both groups presented motor IS below 85 at 3^rd month of age. It is important to note that infants scored below the BSID-II mean for the period measured. Although the SGA group presented lower mean motor scores compared to the AGA group at 3 months of life. There were not differences between SGA and AGA groups.

Table 3 shows the distribution of frequency for each item successfully performed by SGA and AGA groups. There were differences between SGA and AGA groups for the item "reaches for suspended ring". The SGA group showed higher frequency in comparison with the AGA group.

Discussion

The assessment and detection of children with less obvious delays of development in the first trimester of life can be a challenge for health professionals and researchers, because such disabilities only become obvious gradually over time^{(19, 20)}. Therefore, the present cross-sectional study compared the fine motor skills of full-term SGA with AGA infants in the 3^rd month of life.

In this study the SGA and AGA groups had homogeneous distribution for profiles of birth conditions of the infants, except for birthweight. These results indicate the effectiveness of the method used for subject selection and classification into the groups. Regarding to family characteristics, there was a greater frequency of SGA group mothers who presented fewer than 8 years of study (81%) and did not work outside of the home (85%). Taking into account that parents tend to be super-protective and cautious when their children have some biological risk^{(25, 26)}, and that children whose mothers with a lower level of education are less likely to be stimulated⁽²⁷⁾, these factors could have influenced negatively the performance of the SGA group.

SGA and AGA groups were similar regarding to mental and motor IS in the 3^rd month. The same results were also observed between other studies, not showing differences in cognitive and motor developments between SGA and AGA groups^(28,29). Conversely, some studies have found significant differences between SGA and AGA infants concerning neurodevelopment⁽³⁰⁾, attention/arousal and motor quality⁽⁶⁾, and cognitive and school performances^{(31, 32)}. The conflicting results probably occur because of the heterogeneity of the groups from one study to another. In some studies, newborns with risk factors for developmental abnormalities were included; in others, preterm SGA newborns were selected. Moreover, a variety of developmental characteristics and assessment at different ages were investigated⁽³³⁾.

Concerning a series of items administered to investigate fine motor skills, there was a significant difference in the item "reaches for suspended ring", i.e. the SGA group (22.2%) showed higher frequency in comparison with the AGA group (2.3%). However, most SGA (77.8%) and AGA (97.7 %) infants did not accomplish this item in the 3^rd month.

To give credit in the execution of this item the infant must move their arm(s) in the ring direction while looking at the ring. To try to understand the highest score of the SGA group in this situation we pointed for one situation. Full-term SGA infants shows greater movement of the arms compared to the control group⁽³⁴⁾, which may have led the SGA group to launch his arm(s) toward the ring accidentally, with no real purpose to achieve it, more often than the AGA group.

This fact observed in the item "reaches for suspended ring" does not mean a better performance of the SGA group compared to the AGA group, since in the other assessed items ("manipulates ring"; "grasps suspended ring"; "carries ring to mouth"), there were no significant difference between groups. Probably, these items require higher skills ('manipulation', 'reach', followed by 'carries the object to mouth') and consequently the SGA group found them more difficult to perform. In these items, since the increased arm movement frequency is not enough. In these items, a higher level of fine motor skills is necessary and only the increased arm(s) movement frequency was not enough to maintain the SGA group higher frequency in comparison with the AGA group.

Similar results were found when visual function and fine motor control were compared using BSID-II in the first semester of life. The SGA group showed higher frequency of fine motor control items in the 1^st month ("attempts to bring hands to mouth") and in the ^3rd month ("reaches for suspended ring"). Those differences were attributed to a great speed and great occurrence of arm movements observed in SGA group⁽⁷⁾. The literature points out to differences in the quality of movement, corroborating this explanation. It has been reported an increased incidence of convulsive movements, jerking and trembling in full-term SGA infants⁽³⁴⁾. These movements have been described as "windmill motions of the arms"⁽³⁵⁾, or "wind-milling arm movement"⁽³⁶⁾, or "cycling movements"⁽³⁷⁾, or "arm movements in circles"⁽³⁸⁾.

The BSID-II results for the studied sample showed that the infants were within the normal range concerning mental IS (100±15). Conversely, regarding motor IS, the infants scored below the BSID-II mean at the 3^rd month, at least lower than expected for typical well-developing infants. This raises the question of what might account for this difference. The lack of validation of the developmental tests in developing countries may have contributed to the disadvantages observed in the groups studied⁽³⁹⁾.

From a longitudinal study with monthly monitoring of the 1^st to the 12^th month of age, Santos, Gabbard and Gonçalves (2001)⁽³⁹⁾ investigated the characteristics of motor development in Brazilian children during the first year of life by comparing the results with the North American sample used in the validation of the BSID-II. Although the results were similar in most months, the Brazilian sample showed significantly lower mean score than the North American sample in the 3^rd, 4^th and 5^th month, especially related to the skills to sit and hold. It is argued that the differences may be related to differences in practices used in daily care with Brazilian infants reflected in lower scores on scales not validated in Brazil⁽³⁹⁾. Likewise, it is suggested that the differences found in the 3rd month in both groups may be a reflection of not validating the BSID-II in our country.

The present study has certain limitations that need to be taken into. First, the cross-sectional design does not permit analysis of changes over time. Second the sample size could at least in part influence the results. A larger sample should be considered in future research. Third, this was a quantitative study of some aspects of the fine motor skill. Future research should be directed to evaluate other facets, such as quality and frequency of arm movement. Fourth, there are conflicting results in the literature regarding neurodevelopment of infants exposed to intrauterine malnutrition⁽³³⁾ because of the heterogeneity of the groups studied (inclusion of premature newborns), different assessment instruments and the duration of the follow-up period.

The results indicate that intrauterine malnutrition may have influenced the fine motor skills in the infants studied, with a need for greater attention concerning the development of SGA infants. Whether such difference found at 3^rd month is of clinical significance is uncertain, as well as its influence on future fine motor skills. For the sample studied, SGA and AGA groups were similar regarding mental and motor IS in the 3^rd month. There was a significant difference for fine motor skills between the groups when observing the item "reaches for suspended ring". We hypothesize that this difference could be attributed to a greater occurrence of arm movement observed in the SGA group and not to a better motor performance of this group.

Acknowledgements

We are thankful to the parents and their infants for agreeing to participate in this study. This research was supported by the State of São Paulo Research Foundation (Fapesp), under document no. 00/07234 and Coordination for the Improvement of Higher Education Personnel (CAPES). We would also like to thank the involvement of the Division of Neonatology, Department of Pediatrics, Center for Investigation in Pediatrics (Ciped) and the Department of Neurology of the Faculty of Medical Sciences/Unicamp.

References

• 1. Levitsky DA, Strupp BJ. Malnutrition and the brain: changing concepts, changing concerns. J Nutr 1995;125:2212S-2220S.
• 2. de Onis M, Blössner M, Villar J. Levels and patterns of intrauterine growth retardation in developing countries. Eur J Clin Nutr 1998;52Suppl 1:S5-15.
• 3. Sommerfelt K, Andersson HW, Sonnander K, Ahlsten G, Ellertsen B, Markestad T et al Cognitive development of term small for gestational age children at five years of age. Arch Dis Child 2000;83:25-30.
• 4. Grantham-McGregor SM, Lira PI, Ashworth A, Morris SS, Assunçao AM. The development of low birth weight term infants and the effects of the environment in northeast Brazil. J Pediatr 1998;132:661-6.
• 5. Eickmann SH, Lira PI, Lima MC. Desenvolvimento mental e motor aos 24 meses de crianças nascidas a termo com baixo peso. Arq Neuropsiquiatr 2002;60:748-54.
• 6. Mello BB, Gonçalves VM, Souza EA. Behavior of full term infants small for gestational age in the first three months of life. Arq Neuropsiquiatr 2004;62:1046-51.
• 7. Gagliardo HG, Gonçalves VM, Lima MC, Francozo Mde F, Aranha Netto A. Visual function and fine-motor control in small-for-gestational age infants. Arq Neuropsiquiatr 2004;62:955-62.
• 8. Goto MM, Gonçalves VM, Netto AA, Morcillo AM, Moura-Ribeiro MV. Neurodevelopment of full-term small-for-gestational age infants in the second month of life. Arq Neuropsiquiatr 2005;63:75-82.
• 9. Campos D, Santos DC, Goncalves VM, Goto MM, Campos-Zanelli TM. Motor performance of infants born small or appropriate for gestational age: a comparative study. Pediatr Phys Ther 2008;20:340-6.
• 10. Azenha VM, Mattar MA, Cardoso VC, Barbieri MA, Del Ciampo LA, Bettiol H. Peso insuficiente ao nascer: estudo de fatores associados em duas coortes de recém-nascidos em Ribeirão Preto, São Paulo. Rev Paul Pediatr 2008;26:27-35.
• 11. Strauss RS. Adult functional outcome of those born small for gestational age: twenty-six-year follow-up of the 1970 British Birth Cohort. JAMA 2000;283:625-32.
• 12. Sommerfelt K, Sonnander K, Skranes J, Andersson HW, Ahlsten G, Ellertsen B et al Neuropsychologic and motor function in small-for-gestation preschoolers. Pediatr Neurol 2002;26:186-91.
• 13. Markestad T, Vik T, Ahlsten G, Gebre-Medhin M, Skjaerven R, Jacobsen G et al Small-for-gestational-age (SGA) infants born at term: growth and development during the first year of life. Acta Obstet Gynecol Scand Suppl 1997;165:93-101.
• 14. Evensen KA, Skranes J, Brubakk AM, Vik T. Predictive value of early motor evaluation in preterm very low birth weight and term small for gestational age children. Early Hum Dev 2009;85:511-8.
• 15. Corbetta D, Snapp-Childs W. Seeing and touching: the role of sensory-motor experience on the development of infant reaching. Infant Behav Dev 2009;32:44-58.
• 16. Feder KP, Majnemer A. Handwriting development, competency, and intervention. Dev Med Child Neurol 2007;49:312-7.
• 17. Groen SE, de Blécourt AC, Postema K, Hadders-Algra M. General movements in early infancy predict neuromotor development at 9 to 12 years of age. Dev Med Child Neurol 2005;47:731-8.
• 18. Bouwstra H, Dijk-Stigter GR, Grooten HM, Janssen-Plas FE, Koopmans AJ, Mulder CD et al. Prevalence of abnormal general movements in three-month-old infants. Early Hum Dev 2009;85:399-403.
• 19. Einspieler C, Prechtl HF, Ferrari F, Cioni G, Bos AF. The qualitative assessment of general movements in preterm, term and young infants - review of the methodology. Early Hum Dev 1997;50:47-60.
• 20. Spittle AJ, Doyle LW, Boyd RN. A systematic review of the clinimetric properties of neuromotor assessments for preterm infants during the first year of life. Dev Med Child Neurol 2008;50:254-66.
• ²¹
  Organização Mundial da Saúde. Classificação Estatística Internacional de Doenças e Problemas Relacionados à Saúde. 10ª revisão. 7ª ed. v. 1. São Paulo: Editora da Universidade São Paulo; 1999. p. 1181-6.
• 22. Battaglia FC, Lubchenco LO. A practical classification of newborn infants by weight and gestational age. J Pediatr 1967;71:159-63.
• 23. Eickmann SH, Maciel AM, Lira PI, Lima MC. Factors associated with mental and psychomotor development of infants in four public day care centers in the municipality of Recife, Brazil. Rev Paul Pediatr 2009;27:282-8.
• 24. Bayley N. Bayley Scales on Infant Development. Manual. 2nd ed. San Antonio (TX): The Psychological Corporation; 1993.
• 25. Aylward GP, Pfeiffer SI, Wright A, Verhulst SJ. Outcome studies of low birth weight infants published in the last decade: a metaanalysis. J Pediatr 1989;115:515-20.
• 26. Bjerre I, Hansen E. Psychomotor development and school-adjustment of 7-year-old children with low birthweight. Acta Paediatr Scand 1976;65:88-96.
• 27. Watt J, Strongman KT. Mother-infant interactions at 2 and 3 months in preterm, small-for-gestational-age, and full-term infants; their relationship with cognitive development at 4 months. Early Hum Dev 1985;11:231-46.
• 28. Newman DG, O'Callaghan MJ, Harvey JM, Tudehope DI, Gray PH, Burns YR et al Characteristics at four months follow-up of infants born small for gestational age: a controlled study. Early Hum Dev 1997;49:169-81.
• 29. Cruz-Martinez R, Figueras F, Oros D, Padilla N, Meler E, Hernandez-Andrade E et al Cerebral blood perfusion and neurobehavioral performance in full-term small-for-gestational-age fetuses. Am J Obstet Gynecol 2009;201:474-7.
• 30. Paz I, Gale R, Laor A, Danon YL, Stevenson DK, Seidman DS. The cognitive outcome of full-term small for gestational age infants at late adolescence. Obstet Gynecol 1995;85:452-6.
• 31. Larroque B, Bertrais S, Czernichow P, Léger J. School difficulties in 20-year-olds who were born small for gestational age at term in a regional cohort study. Pediatrics 2001;108:111-5.
• 32. Bos AF, Einspieler C, Prechtl HF. Intrauterine growth retardation, general movements, and neurodevelopmental outcome: a review. Dev Med Child Neurol 2001;43:61-8.
• 33. van Kranen-Mastenbroek VH, Kingma H, Caberg HB, Ghys A, Blanco CE, Hasaart TH et al Quality of spontaneous general movements in full-term small for gestational age and appropriate for gestational age newborn infants. Neuropediatrics 1994;25:145-53.
• 34. Michaelis R, Schulte FJ, Nolte R. Motor behavior of small for gestational age newborn infants. J Pediatr 1970;76:208-13.
• 35. Amiel-Tison C, Grenier A, Goldberg R. Neurological assessment during the first year of life. New York: Oxford University Press; 1986.
• 36. Dubowitz LM, Dubowitz V, Mercuri E. The neurological assessment of the preterm and full-term newborn infant. 2^nd ed. Cambridge: University Press; 2000.
• 37. Einspieler C, Cioni G, Paolicelli PB, Bos AF, Dressler A, Ferrari F et al The early markers for later dyskinetic cerebral palsy are different from those for spastic cerebral palsy. Neuropediatrics 2002;33:73-8.
• 38. Santos DC, Gabbard C, Gonçalves VM. Motor development during the first year: a comparative study. J Genet Psychol 2001;162:143-53.

Small-for-gestational-age newborn infant: repercussion on fine motor skills

Pequeño para la edad gestacional: repercusión en las habilidades motoras finas

Publication Dates

• Publication in this collection
  26 Apr 2011
• Date of issue
  Mar 2011

History

• Accepted
  12 July 2010
• Received
  03 Feb 2010