ABSTRACT

Abnormal general movements are among the most reliable markers for cerebral palsy. General movements are part of the spontaneous motor repertoire and are present from early fetal life until the end of the first half year after term. In addition to its high sensitivity (98%) and specificity (91%), the assessment of general movements is non-invasive and time- and cost-efficient. It is therefore ideal for assessing the integrity of the young nervous system, most notably in lowresource settings. Studies on the general movements assessment in low- and middle-income countries such as China, India, Iran, or South Africa are still rare but increasing. In Brazil, too, researchers have demonstrated that the evaluation of general movements adds to the functional assessment of the young nervous system. Applying general movements assessment in vulnerable populations in Brazil is therefore highly recommended.

DESCRIPTORS
Infant; Premature; Cerebral Palsy; Psychomotor Disorders; Psychomotor Performance; Motor Activity; Disability Evaluation

INTRODUCTION

One of the most challenging tasks for medical practitioners is to identify specific risk factors in early infancy and to reliably predict impairment that manifests later in life. Cerebral palsy (CP) is one such condition that usually manifests before 18 months of age⁴²42. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, et al. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl. 2007;49(s109):8-14. https://doi.org/10.1111/j.1469-8749.2007.tb12610.x
https://doi.org/10.1111/j.1469-8749.2007... , with an overall prevalence of 2.11 per 1,000 live births³⁷37. Oskoui M, Coutinho F, Dykeman J, Jette N, Pringsheim T. An update on the prevalence of cerebral palsy: a systematic review and meta-analysis. Dev Med Child Neurol. 2013;55(6):509-19. https://doi.org/10.1111/dmcn.12080
https://doi.org/10.1111/dmcn.12080... , increasing to over 10% with decreasing gestational age²⁹29. Himpens E, Van den Broeck C, Oostra A, Calders P, Vanhaesebrouck P. Prevalence, type, distribution, and severity of cerebral palsy in relation to gestational age: a meta-analytic review. Dev Med Child Neurol. 2008;50(5):334-40. https://doi.org/10.1111/j.1469-8749.2008.02047.x
https://doi.org/10.1111/j.1469-8749.2008... . As CP affects a number of functional and medical domains, it poses various challenges to affected children, their families, and healthcare, especially in low- and middle-income countries (LMIC), according to the World Bank country classification⁴⁸48. World Health Organization. Health statstics and information systems: definition of region groupings. Geneva: WHO; 2016 [cited 2016 Oct 28]. Available from: http://www.who.int/healthinfo/global_burden_disease/definition_regions/en/
http://www.who.int/healthinfo/global_bur... .

There is increasing evidence for the importance of early intervention in children with motor delays. Simply put: the sooner the intervention, the better the outcome³⁵35. Noritz GH, Murphy NA. Neuromotor Screening Expert Panel. Motor delays: early identification and evaluation. Pediatrics. 2013;131(6):e2016-e2027. https://doi.org/www.pediatrics.org/cgi/content/full/131/6/e2016
https://doi.org/www.pediatrics.org/cgi/c... . But CP diagnosis can be tedious and difficult, particularly when human and financial healthcare resources are limited. The LMIC are struggling to provide expensive medical equipment for diagnoses, such as magnetic resonance imaging, computed tomography or cranial ultrasonography. The general movement assessment (GMA, see below) is cost- and time-efficient. Due to its high predictive value (sensitivity 98% [95%CI 74–100]; specificity 91% [95%CI 83–93])⁴4. Bosanquet M, Copeland L, Ware R, Boyd R. A systematic review of tests to predict cerebral palsy in young children. Dev Med Child Neurol. 2013;55(5):418-26. https://doi.org/10.1111/dmcn.12140
https://doi.org/10.1111/dmcn.12140... , it is used by an ever-increasing number of health professionals around the world for early identification of infants with a high risk for CP⁴4. Bosanquet M, Copeland L, Ware R, Boyd R. A systematic review of tests to predict cerebral palsy in young children. Dev Med Child Neurol. 2013;55(5):418-26. https://doi.org/10.1111/dmcn.12140
https://doi.org/10.1111/dmcn.12140... ^,1414. Einspieler C, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Prechtl's method on the qualitative assessment of general movements in preterm, term and young infants. London: Mac Keith Press; 2004..

What are General Movements?

Fetuses and young infants display a large repertoire of spontaneous movements such as stretching, yawning, twitching, and a specific motor pattern commonly known as general movements (GM). GM are complex and involve the entire body, notably arm, leg, neck, and trunk movements. They include rotations and vary in speed, intensity, and direction, which makes them appear elegant and fluent. GM emerge at nine weeks postmenstrual age (fetal GM) and continue after birth, with unchanging characteristics at first¹³13. 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(2):73-8. https://doi.org/10.1055/s-2002-32368
https://doi.org/10.1055/s-2002-32368... . So-called preterm GM show no difference to fetal GM. GM that emerge around the term and during the first two months postterm are called writhing movements (WM) – ellipsoidal movements characterized by a small to moderate amplitude and low to moderate speed. At a postterm age of three to five months, WM are gradually replaced by small movements of the neck, trunk, and limbs, which are commonly referred to as fidgety movements (FM)¹⁸18. Einspieler C, Bos AF, Libertus ME, Marschik PB. The general movement assessment helps us to identify preterm infants at risk for cognitive dysfunction. Front Psychol. 2016;7:406. https://doi.org/10.3389/fpsyg.2016.00406
https://doi.org/10.3389/fpsyg.2016.00406... . Finally, with the onset of intentional and anti-gravity movements, GM gradually disappear towards the end of the first half-year of life¹⁴14. Einspieler C, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Prechtl's method on the qualitative assessment of general movements in preterm, term and young infants. London: Mac Keith Press; 2004.^,1515. Einspieler C, Prechtl HFR. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11(1):61-7. https://doi.org/10.1002/mrdd.20051
https://doi.org/10.1002/mrdd.20051... .

The General Movement Assessment

Evaluating the quality of age-specific GM by GMA¹⁵15. Einspieler C, Prechtl HFR. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11(1):61-7. https://doi.org/10.1002/mrdd.20051
https://doi.org/10.1002/mrdd.20051... mainly serves to predict or rule out neurological impairments that become manifest only later in life (e.g., CP). In a systematic review of assessment techniques for predicting CP, GMA was found to be better suited than cranial ultrasound, neurological examination, or even magnetic resonance imaging⁴4. Bosanquet M, Copeland L, Ware R, Boyd R. A systematic review of tests to predict cerebral palsy in young children. Dev Med Child Neurol. 2013;55(5):418-26. https://doi.org/10.1111/dmcn.12140
https://doi.org/10.1111/dmcn.12140... . With summary estimates for sensitivity and specificity of 98% (95%CI 74–100) and 91% (95%CI 83–93), respectively, Bosanquet et al.⁴4. Bosanquet M, Copeland L, Ware R, Boyd R. A systematic review of tests to predict cerebral palsy in young children. Dev Med Child Neurol. 2013;55(5):418-26. https://doi.org/10.1111/dmcn.12140
https://doi.org/10.1111/dmcn.12140... clearly found GMA to be the method of choice.

Applying GMA is straightforward: for a reliable assessment (kappa values ranging from 0.89 to 0.93¹⁵15. Einspieler C, Prechtl HFR. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11(1):61-7. https://doi.org/10.1002/mrdd.20051
https://doi.org/10.1002/mrdd.20051... ), a 3- to 5-minute video of the infant is recorded following few basic principles (e.g., infant lying in supine position, comfortably dressed, not crying)¹²12. Einspieler C, Prechtl HFR, 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(1):47-60. https://doi.org/10.1016/S0378-3782(97)00092-3
https://doi.org/10.1016/S0378-3782(97)00... . Performed by trained GM scorers, the assessment as such can be carried out on site²⁶26. Guzzetta A, Belmonti V, Battini R, Boldrini A, Paolicelli PB, Cioni G. Does the assessment of general movements without video observation reliably predict neurological outcome? Eur J Paediatr Neurol. 2007;11(6):362-7. https://doi.org/10.1016/j.ejpn.2007.03.003
https://doi.org/10.1016/j.ejpn.2007.03.0... or elsewhere; it is time-efficient and incurs minimal costs¹²12. Einspieler C, Prechtl HFR, 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(1):47-60. https://doi.org/10.1016/S0378-3782(97)00092-3
https://doi.org/10.1016/S0378-3782(97)00... . Scorers classify GM as “normal” or “abnormal”. Abnormal preterm GM and WM can be either classified as the following: a) poor repertoire (low complexity and variability, monotony); b) cramped-synchronized (no smoothness, simultaneous contraction and relaxation of the limbs); or c) chaotic (no smoothness, chaotic and abrupt movements of large amplitude)¹⁴14. Einspieler C, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Prechtl's method on the qualitative assessment of general movements in preterm, term and young infants. London: Mac Keith Press; 2004.^,1515. Einspieler C, Prechtl HFR. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11(1):61-7. https://doi.org/10.1002/mrdd.20051
https://doi.org/10.1002/mrdd.20051... .

Abnormal FM can be classified as absent or abnormal in terms of exaggerated jerkiness and speed. Already in 1997, Heinz Prechtl et al.⁴¹41. Prechtl HFR, Einspieler C, Cioni G, Bos AF, Ferrari F, Sontheimer D. An early marker for neurological deficits after perinatal brain lesions. Lancet. 1997;349(9062):1361-3. https://doi.org/10.1016/S0140-6736(96)10182-3
https://doi.org/10.1016/S0140-6736(96)10... demonstrated that normal FM are a highly reliable marker for a normal neurological development even if the medical history and cranial ultrasound had indicated a high risk for maldevelopment. An absence of FM, by contrast, indicates a neurologically adverse development even in infants with no structural impairment⁴¹41. Prechtl HFR, Einspieler C, Cioni G, Bos AF, Ferrari F, Sontheimer D. An early marker for neurological deficits after perinatal brain lesions. Lancet. 1997;349(9062):1361-3. https://doi.org/10.1016/S0140-6736(96)10182-3
https://doi.org/10.1016/S0140-6736(96)10... . These findings have been repeatedly confirmed all over the world²2. Adde L, Thomas N, John HB, Oommen S, Vagen RT, Fjortoft T, et al. Early motor repertoire in very low birth weight infants in India is associated with motor development at one year. Eur J Paediatr Neurol. 2016;20(6):918-24. https://doi.org/10.1016/j.ejpn.2016.07.019
https://doi.org/10.1016/j.ejpn.2016.07.0... ^,99. Burger M, Frieg A, Louw QA. General movements as a predictive tool of the neurological outcome in very low and extremely low birth weight infants: a South African perspective. Early Hum Dev. 2011;87(4):303-8. https://doi.org/10.1016/j.earlhumdev.2011.01.034
https://doi.org/10.1016/j.earlhumdev.201... ^,4949. Yang H, Einspieler C, Shi W, Marschik PB, Wang Y, Cao Y, et al. Cerebral palsy in children: movements and postures during early infancy, dependent on preterm vs. full term birth. Early Hum Dev. 2012;88(10):837-43. https://doi.org/10.1016/j.earlhumdev.2012.06.004
https://doi.org/10.1016/j.earlhumdev.201... ^,5050. Yuge M, Marschik PB, Nakajima Y, Yamori Y, Kanda T, Hirota H, et al. Movements and postures of infants aged 3 to 5 months: to what extent is their optimality related to perinatal events and to the neurological outcome? Early Hum Dev. 2011;87(3):231-7. https://doi.org/10.1016/j.earlhumdev.2010.12.046
https://doi.org/10.1016/j.earlhumdev.201... , with a sensitivity of 91%–98% and a specificity of 81%–91%⁴4. Bosanquet M, Copeland L, Ware R, Boyd R. A systematic review of tests to predict cerebral palsy in young children. Dev Med Child Neurol. 2013;55(5):418-26. https://doi.org/10.1111/dmcn.12140
https://doi.org/10.1111/dmcn.12140... ^,88. Burger M, Louw QA. The predictive validity of general movements: a systematic review. Eur J Paediatr Neurol. 2009;13(5):408-20. https://doi.org/10.1016/j.ejpn.2008.09.004
https://doi.org/10.1016/j.ejpn.2008.09.0... .

Although GMA is based on visual Gestalt perception, attempts were recently made to use computer-based analysis¹1. Adde L, Helbostad JL, Jensenius AR, Taraldsen G, Grunewaldt KH, Stoen R. Early prediction of cerebral palsy by computer-based video analysis of general movements: a feasibility study. Dev Med Child Neurol. 2010;52(8):773-778. https://doi.org/10.1111/j.1469-8749.2010.03629.x
https://doi.org/10.1111/j.1469-8749.2010... ^,1717. Einspieler C, Marschik PB. Complementary thinking: future perspectives on the assessment of general movements. Dev Med Child Neurol. 2013;55(8):682-3. https://doi.org/10.1111/dmcn.12174
https://doi.org/10.1111/dmcn.12174... ^,3434. Marcroft C, Khan A, Embleton ND, Trenell M, Plötz T. Movement recognition technology as a method of assessing spontaneous general movements in high risk infants. Front Neurol. 2014;5:284. https://doi.org/10.3389/fneur.2014.00284
https://doi.org/10.3389/fneur.2014.00284... .

Early Specific Markers for Cerebral Palsy: The Benefits of General Movement Assessment

Already at late preterm age and around term (i.e., at a term-equivalent age) crampedsynchronized GM, if present for several weeks, were found to be highly predictive for spastic CP¹⁵15. Einspieler C, Prechtl HFR. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11(1):61-7. https://doi.org/10.1002/mrdd.20051
https://doi.org/10.1002/mrdd.20051... ^,1616. Einspieler C, Marschik PB, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Early markers for cerebral palsy: insights from the assessment of general movements. Future Neurol. 2012;7(6):709-17. https://doi.org/10.2217/fnl.12.60
https://doi.org/10.2217/fnl.12.60... ^,2121. Ferrari F, Cioni G, Einspieler C, Roversi MF, Bos AF, Paolicelli PB, et al. Cramped synchronized general movements in preterm infants as an early marker for cerebral palsy. Arch Pediatr Adolesc Med. 2002;156(5):460-7. https://doi.org/10.1001/archpedi.156.5.460
https://doi.org/10.1001/archpedi.156.5.4... . At the age of three to five months, it is possible to predict both bilateral and unilateral CP by GMA. Most individuals show no FM, but those who are to develop unilateral CP show initial asymmetries in isolated wrist and finger movements¹¹11. Cioni G, Bos AF, Einspieler C, Ferrari F, Martijn A, Paolicelli PB, et al. Early neurological signs in preterm infants with unilateral intraparenchymal echodensity. Neuropediatrics. 2000;31(5):240-51. https://doi.org/10.1055/s-2000-9233
https://doi.org/10.1055/s-2000-9233... ^,2525. Guzzetta A, Mercuri E, Rapisardi G, Ferrari F, Roversi MF, Cowan F, et al. General movements detect early signs of hemiplegia in term infants with neonatal cerebral infarction. Neuropediatrics. 2003;34(2):61-6. https://doi.org/10.1055/s-2003-39597
https://doi.org/10.1055/s-2003-39597... ^,2727. Guzzetta A, Pizzardi A, Belmonti V, Boldrini A, Carotenuto M, D'Acunto G, et al. Hand movements at 3 months predict later hemiplegia in term infants with neonatal cerebral infarction. Dev Med Child Neurol. 2010;52(8):767-72. https://doi.org/10.1111/j.1469-8749.2009.03497.x
https://doi.org/10.1111/j.1469-8749.2009... . Poor repertoire of GM at term age followed by an absence of FM and circular arm movements can be seen as early markers for dyskinetic CP¹³13. 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(2):73-8. https://doi.org/10.1055/s-2002-32368
https://doi.org/10.1055/s-2002-32368... ^,1616. Einspieler C, Marschik PB, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Early markers for cerebral palsy: insights from the assessment of general movements. Future Neurol. 2012;7(6):709-17. https://doi.org/10.2217/fnl.12.60
https://doi.org/10.2217/fnl.12.60... . A detailed assessment that goes beyond standard GMA can indicate the severity of CP¹⁶16. Einspieler C, Marschik PB, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Early markers for cerebral palsy: insights from the assessment of general movements. Future Neurol. 2012;7(6):709-17. https://doi.org/10.2217/fnl.12.60
https://doi.org/10.2217/fnl.12.60... . Applying Prechtl's optimality concept⁴⁰40. Prechtl HFR. The optimality concept [editorial]. Early Hum Dev. 1980;4(3):201-5. https://doi.org/10.1016/0378-3782(80)90026-2
https://doi.org/10.1016/0378-3782(80)900... , Einspieler et al. presented a motor optimality score based both on standard GMA¹⁴14. Einspieler C, Bos AF, Ferrari F, Cioni G, Prechtl HFR. Prechtl's method on the qualitative assessment of general movements in preterm, term and young infants. London: Mac Keith Press; 2004. and on the assessment of other postures and movements than FM. A low motor optimality score was associated with a limited functional mobility and activity⁷7. Bruggink JL, Cioni G, Einspieler C, Maathuis CG, Pascale R, Bos AF. Early motor repertoire is related to level of self-mobility in children with cerebral palsy at school age. Dev Med Child Neurol. 2009;51(11):878-85. https://doi.org/10.1111/j.1469-8749.2009.03294.x
https://doi.org/10.1111/j.1469-8749.2009... ^,4949. Yang H, Einspieler C, Shi W, Marschik PB, Wang Y, Cao Y, et al. Cerebral palsy in children: movements and postures during early infancy, dependent on preterm vs. full term birth. Early Hum Dev. 2012;88(10):837-43. https://doi.org/10.1016/j.earlhumdev.2012.06.004
https://doi.org/10.1016/j.earlhumdev.201... .

General Movement Assessment in Asian and African Low- and Middle-Income Countries

Its straightforward applicability makes GMA an ideal tool for assessing the young nervous system, all the more so in low-resource settings. But how widespread is GMA in non-European LMIC? To get an idea of the current literature on GMA published in non-European LMIC, we conducted a literature research in PubMed and – for broad coverage – Google Scholar, based on the key terms “general movements” and “general movements assessment”. We then selected English publications with a principal investigator based in an LMIC, according to authorship or the study conducted by them (Box).

In Asia, three Chinese studies³²32. Ma L, Yang B, Meng L, Wang B, Zheng C, Cao A. Effect of early intervention on premature infants’ general movements. Brain Dev. 2015;37(4):387-93. https://doi.org/10.1016/j.braindev.2014.07.002
https://doi.org/10.1016/j.braindev.2014.... ^,4949. Yang H, Einspieler C, Shi W, Marschik PB, Wang Y, Cao Y, et al. Cerebral palsy in children: movements and postures during early infancy, dependent on preterm vs. full term birth. Early Hum Dev. 2012;88(10):837-43. https://doi.org/10.1016/j.earlhumdev.2012.06.004
https://doi.org/10.1016/j.earlhumdev.201... ^,5151. Zang FF, Yang H, Han Q, Cao JY, Tomantschger I, Krieber M, et al. Very low birth weight infants in China: the predictive value of the motor repertoire at 3 to 5 months for the motor performance at 12 months. Early Hum Dev. 2016;100:27-32. https://doi.org/10.1016/j.earlhumdev.2016.03.010
https://doi.org/10.1016/j.earlhumdev.201... , one study conducted in India²2. Adde L, Thomas N, John HB, Oommen S, Vagen RT, Fjortoft T, et al. Early motor repertoire in very low birth weight infants in India is associated with motor development at one year. Eur J Paediatr Neurol. 2016;20(6):918-24. https://doi.org/10.1016/j.ejpn.2016.07.019
https://doi.org/10.1016/j.ejpn.2016.07.0... , and one Iranian study⁴⁵45. Soleimani F, Badv RS, Momayezi A, Biglarian A, Marzban A. General movements as a predictive tool of the neurological outcome in term born infants with hypoxic ischemic encephalopathy. Early Hum Dev. 2015;91(8):479-2. https://doi.org/10.1016/j.earlhumdev.2015.05.007
https://doi.org/10.1016/j.earlhumdev.201... met the inclusion criteria. Yang et al.⁴⁹49. Yang H, Einspieler C, Shi W, Marschik PB, Wang Y, Cao Y, et al. Cerebral palsy in children: movements and postures during early infancy, dependent on preterm vs. full term birth. Early Hum Dev. 2012;88(10):837-43. https://doi.org/10.1016/j.earlhumdev.2012.06.004
https://doi.org/10.1016/j.earlhumdev.201... conducted a longitudinal assessment in a large number of children, confirming that the absence of FM was a significant marker of CP. It was also one of the first studies to find that a detailed assessment of postures and movements other than FM helps to predict CP severity. Although more than 100,000 infants with very low birth weight are born annually in China³¹31. Liu J, Huang L, Yan H, Chen H, Guo J. [Morbidity and mortality outcomes for very low birth weight infants from a single center during 2009-2010]. Chin J Neonatol. 2012;4:243-6. Chinese., studies on their early motor performance are still scarce. Recently, Zang et al.⁵¹51. Zang FF, Yang H, Han Q, Cao JY, Tomantschger I, Krieber M, et al. Very low birth weight infants in China: the predictive value of the motor repertoire at 3 to 5 months for the motor performance at 12 months. Early Hum Dev. 2016;100:27-32. https://doi.org/10.1016/j.earlhumdev.2016.03.010
https://doi.org/10.1016/j.earlhumdev.201... demonstrated that both absent FM and a low MOS were associated with a poor or even very poor gross and fine motor performance at 12 months corrected age. Such an early identification enables early intervention programmes before pathological features become manifest. In Jinan and Binzou, Ma et al.³²32. Ma L, Yang B, Meng L, Wang B, Zheng C, Cao A. Effect of early intervention on premature infants’ general movements. Brain Dev. 2015;37(4):387-93. https://doi.org/10.1016/j.braindev.2014.07.002
https://doi.org/10.1016/j.braindev.2014.... showed that early intervention by auditory stimulation, visual stimulation, tactile stimulation, vestibular motion stimulation, pediatric gymnastics, or hydrotherapy improves GM. Apart from these publications, a considerable number of Chinese rehabilitation doctors, neurologists, pediatricians, and physiotherapists constantly exchange their experiences with GMA online (http://www.gmshome.cn). Another study on VLBW infants and their GM was recently conducted in India, applying both visual perception-based and computer-based GMA²2. Adde L, Thomas N, John HB, Oommen S, Vagen RT, Fjortoft T, et al. Early motor repertoire in very low birth weight infants in India is associated with motor development at one year. Eur J Paediatr Neurol. 2016;20(6):918-24. https://doi.org/10.1016/j.ejpn.2016.07.019
https://doi.org/10.1016/j.ejpn.2016.07.0... . Similar to Zang et al.⁵¹51. Zang FF, Yang H, Han Q, Cao JY, Tomantschger I, Krieber M, et al. Very low birth weight infants in China: the predictive value of the motor repertoire at 3 to 5 months for the motor performance at 12 months. Early Hum Dev. 2016;100:27-32. https://doi.org/10.1016/j.earlhumdev.2016.03.010
https://doi.org/10.1016/j.earlhumdev.201... , the Indian study showed that absent or abnormal FM and a monotonously abnormal movement character was associated with lower motor quotients at 12 months corrected age. The computer-based GMA confirmed that the variability of the spatial center of motion was higher – thus indicating absent FM – in children with lower motor quotients²2. Adde L, Thomas N, John HB, Oommen S, Vagen RT, Fjortoft T, et al. Early motor repertoire in very low birth weight infants in India is associated with motor development at one year. Eur J Paediatr Neurol. 2016;20(6):918-24. https://doi.org/10.1016/j.ejpn.2016.07.019
https://doi.org/10.1016/j.ejpn.2016.07.0... .

One of the recent studies on GMA was carried out in Iran. It confirmed the importance of FM observation: according to Soleimani et al.⁴⁵45. Soleimani F, Badv RS, Momayezi A, Biglarian A, Marzban A. General movements as a predictive tool of the neurological outcome in term born infants with hypoxic ischemic encephalopathy. Early Hum Dev. 2015;91(8):479-2. https://doi.org/10.1016/j.earlhumdev.2015.05.007
https://doi.org/10.1016/j.earlhumdev.201... , absent FM indicated a high risk for maldevelopment in a group of infants with perinatal asphyxia.

A similar association between FM and the 12-month outcome was reported from South Africa. In a group of 115 very low birth weight infants, absent FM identified individuals who would perform poorly at the neurodevelopmental and motor assessments around nine months later⁹9. Burger M, Frieg A, Louw QA. General movements as a predictive tool of the neurological outcome in very low and extremely low birth weight infants: a South African perspective. Early Hum Dev. 2011;87(4):303-8. https://doi.org/10.1016/j.earlhumdev.2011.01.034
https://doi.org/10.1016/j.earlhumdev.201... .

General Movement Assessment in Brazil

According to the Brazilian Ministry of Health⁶6. Brasil, Ministério da Saúde. DATASUS: Informações de saúde 2015. Brasília (DF); 2015 [cited 2016 Oct 28]. Available from: http://www2.datasus.gov.br/DATASUS/index.php?area=020
http://www2.datasus.gov.br/DATASUS/index... , pre- and perinatal care in the country is still insufficient, with significant impacts on mother-child health. Poor environmental sanitation and malnutrition are the main causes of Brazil's infant mortality (infant mortality rate in 2015: 13.82 deaths per 1,000 live births)³⁰30. Instituto Brasileiro de Geografia e Estatistica. Brasil em síntese: população: taxas de mortalidade infantil. Rio de Janeiro: IBGE; c2017 [cited 2017 Apr 4]. Available from: http://brasilemsintese.ibge.gov.br/populacao/taxas-de-mortalidade-infantil.html
http://brasilemsintese.ibge.gov.br/popul... and early childhood diseases⁴⁶46. UNICEF. Situação mundial da infância. 2013: crianças com deficiência: resumo executivo. Brasília (DF): UNICEF Brasil; 2013 [cited 2015 Oct 28]. Available from: http://www.unicef.org/brazil/pt/PT_SOWC2013ResumoExecutivo.pdf
http://www.unicef.org/brazil/pt/PT_SOWC2... . Preventive healthcare and early diagnosis of neurodevelopmental disorders are not yet common in the whole country, especially among the vulnerable population. Childhood disabilities are mainly attributable to a poor economic state in association with the parents’ low educational status and nutritional stunting⁴⁴44. Secretaria Municipal de Saúde de Belém (PA). Plano Municipal de Saúde de 2000. Belém; SESMA; 2000.^,4646. UNICEF. Situação mundial da infância. 2013: crianças com deficiência: resumo executivo. Brasília (DF): UNICEF Brasil; 2013 [cited 2015 Oct 28]. Available from: http://www.unicef.org/brazil/pt/PT_SOWC2013ResumoExecutivo.pdf
http://www.unicef.org/brazil/pt/PT_SOWC2... . In order to improve the situation, social protection initiatives for infants and young children with an increased risk for developmental delay or impairment have been implemented. Government grants facilitate the access to healthcare, education, transportation, and recreation⁶6. Brasil, Ministério da Saúde. DATASUS: Informações de saúde 2015. Brasília (DF); 2015 [cited 2016 Oct 28]. Available from: http://www2.datasus.gov.br/DATASUS/index.php?area=020
http://www2.datasus.gov.br/DATASUS/index... . A major aim is to improve child development, but when the diagnosis is delayed, many families have no access to most healthcare services and health promotion strategies.

An effective strategy to identify developmental delay is to conduct consecutive assessments³⁶36. Oliveira MC, Cordani LK. Correlação entre habilidades funcionais referidas pelo cuidador e nível de assistência fornecida a crianças com paralisia cerebral. Temas Desenv. 2002;10(60):15-20.. GMA has so far been performed by a group of specifically trained Brazilian therapists. They apply GMA in maternity wards and hospitals (mainly secondary and tertiary care), but few scientific studies on GM are published⁵5. Brasil P, Pereira Jr JP, Moreira ME, Ribeiro Nogueira RM, Damasceno L, Wakimoto M, et al. Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med. 2016;375(24):2321-34. https://doi.org/10.1056/NEJMoa1602412
https://doi.org/10.1056/NEJMoa1602412... ^,2424. Garcia JM, Gherpelli JLD, Leone CR. The role of spontaneous general movement assessment in the neurological outcome of cerebral lesions in preterm infants. J Pediatr (Rio J). 2004;80(4):296-304. https://doi.org/10.2223/1203
https://doi.org/10.2223/1203... ^,3333. Manacero SA, Marschik PB, Nunes ML, Einspieler C. Is it possible to predict the infant's neurodevelopmental outcome at 14 months of age by means of a single preterm assessment of General Movements? Early Hum Dev. 2012;88(1):39-43. https://doi.org/10.1016/j.earlhumdev.2011.06.013
https://doi.org/10.1016/j.earlhumdev.201... ^,4343. Santos RS, Araújo APQC, Porto MAS. Early diagnosis of abnormal development of preterm newborns: assessment instruments. J Pedriatr (Rio J). 2008;84(4):289-99. https://doi.org/10.1590/S0021-75572008000400003
https://doi.org/10.1590/S0021-7557200800... . In 2008, Santos et al.⁴³43. Santos RS, Araújo APQC, Porto MAS. Early diagnosis of abnormal development of preterm newborns: assessment instruments. J Pedriatr (Rio J). 2008;84(4):289-99. https://doi.org/10.1590/S0021-75572008000400003
https://doi.org/10.1590/S0021-7557200800... discussed various assessment techniques for preterm infants and found GMA to be a reliable and efficient evaluation method (sensitivity 100%, specificity 96%, inter-scorer reliability 92% to 97%). Four years earlier, Garcia et al.²⁴24. Garcia JM, Gherpelli JLD, Leone CR. The role of spontaneous general movement assessment in the neurological outcome of cerebral lesions in preterm infants. J Pediatr (Rio J). 2004;80(4):296-304. https://doi.org/10.2223/1203
https://doi.org/10.2223/1203... had demonstrated, in a sample of 124 preterm infants born in São Paulo, that normal GM were highly predictive of a normal outcome, while only a few infants with abnormal GM developed normally. Furthermore, the authors reported on a high sensitivity (86%) but lower specificity (53%) for GMA, whereas the cranial ultrasound examination revealed the opposite (sensitivity 60%; specificity 87%). They concluded that both assessment tools should be combined²⁴24. Garcia JM, Gherpelli JLD, Leone CR. The role of spontaneous general movement assessment in the neurological outcome of cerebral lesions in preterm infants. J Pediatr (Rio J). 2004;80(4):296-304. https://doi.org/10.2223/1203
https://doi.org/10.2223/1203... . In 2012, Manacero et al.³³33. Manacero SA, Marschik PB, Nunes ML, Einspieler C. Is it possible to predict the infant's neurodevelopmental outcome at 14 months of age by means of a single preterm assessment of General Movements? Early Hum Dev. 2012;88(1):39-43. https://doi.org/10.1016/j.earlhumdev.2011.06.013
https://doi.org/10.1016/j.earlhumdev.201... questioned whether a single preterm assessment of GM could predict the neurodevelopmental outcome at an age of 14 months. The study was carried out in Porto Alegre, RS, Southern Brazil, and comprised of 37 preterm infants whose GM were assessed at 34 weeks postmenstrual age. Children with cramped-synchronized GM had lower percentile ranks in the Alberta Infant Motor Scales at 14 months than children with poor repertoire or normal GM. The study showed that a single assessment of GM during preterm age was only fairly to moderately associated with the motor outcome at 14 months³³33. Manacero SA, Marschik PB, Nunes ML, Einspieler C. Is it possible to predict the infant's neurodevelopmental outcome at 14 months of age by means of a single preterm assessment of General Movements? Early Hum Dev. 2012;88(1):39-43. https://doi.org/10.1016/j.earlhumdev.2011.06.013
https://doi.org/10.1016/j.earlhumdev.201... . In addition, we know that at school age the cognitive and behavioral disabilities can be evidence in infants that were born premature. Only recently, the GMA has also shown its merit for identifying preterm infants at risk for cognitive dysfunction. A normalization of GM before or at term age was associated with higher intelligence quotients at school age compared to a normalization of GM around three to four months postterm age¹⁹19. Einspieler C, Peharz R, Marschik PB. Fidgety movements – tiny in appearance, but huge in impact. J Pediatr (Rio J). 2016;92(3 Supl 1):S64-S70. https://doi.org/10.1016/j.jped.2015.12.003
https://doi.org/10.1016/j.jped.2015.12.0... . This clearly indicates the need for serial GMA. Recently, the very first infants intrauterinely exposed to Zika Virus have been evaluated by GMA. The analysis revealed an exceedingly high percentage of abnormal GM⁵5. Brasil P, Pereira Jr JP, Moreira ME, Ribeiro Nogueira RM, Damasceno L, Wakimoto M, et al. Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med. 2016;375(24):2321-34. https://doi.org/10.1056/NEJMoa1602412
https://doi.org/10.1056/NEJMoa1602412... .

Future Prospects for General Movement Assessment in Brazil

The School of Public Health at the Universidade de São Paulo has recently proposed various studies based on GMA. Identifying high-risk infants at an early stage facilitates the implementation of public health follow-up strategies to provide early care. The proposed studies will comprise infants who: are from families with a vulnerable social background; were intrauterinely exposed to substance abuse; were intrauterinely exposed to malaria or infants with neonatal malaria (both are still common in the indigenous population in northwestern Brazil); or have Down syndrome. In addition, an ongoing collaboration between the University of California, Los Angeles (USA), the Fundação Oswaldo Cruz in Rio de Janeiro, the Universidade de São Paulo, and the Medical University of Graz (Austria) revealed first insights, using GMA, into the early neurological development of infants intrauterinely exposed to Zika Virus⁵5. Brasil P, Pereira Jr JP, Moreira ME, Ribeiro Nogueira RM, Damasceno L, Wakimoto M, et al. Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med. 2016;375(24):2321-34. https://doi.org/10.1056/NEJMoa1602412
https://doi.org/10.1056/NEJMoa1602412... . These ongoing projects, together with the annually organized GMA training courses, will expand the use of GMA in high-risk populations in Brazil. Clinically, GMA can assist in the prediction of cerebral palsy, which allows for the benefits of early intervention to be provided.

The ongoing studies in Brazil will be joint projects of experts of various scientific disciplines in order to strengthen research on child development in vulnerable populations. In addition to the Brazilian researchers’ efforts, a research unit in Graz, Austria, is currently working on the smartphone-based mobile solution “GMApp” (http://gmapp.idn-research.org), which will significantly facilitate GMA in remote areas. Hopefully, the new technology will gain a substantial foothold in Brazil.

CONCLUSION

Developmental assessment based on GM considerably facilitates infant screenings aimed at early detection of developmental abnormalities. However, the use of GMA in LMIC such as Brazil still needs a lot of promotion. The objective remains to initiate early intervention and improve future prospects for children at risk for CP worldwide.

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