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Hypotonia: is it a clear term and an objective diagnosis? An exploratory systematic review

Open AccessPublished:November 07, 2022DOI:https://doi.org/10.1016/j.pediatrneurol.2022.11.001

      ABSTRACT

      Purpose

      Hypotonia is considered a determinant factor in multiple developmental disorders and is associated with various characteristics and morbidities. It is necessary to perform a systematic review to know which characteristics are described as associated with hypotonia in children and which methods are used for its diagnosis.

      Method

      PRISMA guidelines were used to develop the systematic review protocol. A search of databases (Pubmed, Cochrane, Web of Knowledge, among others) was performed in May 2021 to identify relevant studies. Those describing characteristics or tests of hypotonia assessment were included, excluding those that exclusively addressed peripheral hypotonia. Two reviewers evaluated the articles and collected the data in a table, noting the authors, date of publication, type of study, and characteristics or tests described in relation to hypotonia. The quality of the studies was also assessed, and data were extracted.

      Results

      A total of 8,778 studies were identified and analized, of which 45 met the inclusion criteria. Fifty-three characteristics associated with hypotonia, and tests used for its evaluation were located, with pull to sit and vertical suspension being the most frequently referenced.

      Conclusion

      The characteristics associated with hypotonia, more highly debated by authors are muscle strength, hypermobility or the maintenance of antigravity postures. The most used test in the diagnosis of hypotonia is observation, followed by the pull to sit test and adoption of frog posture. A unanimous understanding of the term hypotonia would favor further research.

      Keywords

      INTRODUCTION

      Hypotonia is a frequently used term classified by the WHO under muscle tone disorders of the newborn with code KB08.2

      World Health Organization. ICD-11 International Classification of Diseases 11th Revision [Internet]: WHO; 2018 [updated Feb 2022; cited 2022 Apr 10] Available from: https://icd.who.int/browse11/l-m/en#/http://id.who.int/icd/entity/1830491492

      and in the International Classification of Diseases (ICD-10) with code P94

      Ministerio de Sanidad. eCIEMaps. eCIE10. [Internet]. España: Secretaría General de Salud Digital. 2009 [updated 2010 May 1; cited 2022 Apr 10] Available from: https://eciemaps.mscbs.gob.es/ecieMaps/browser/index_10_2008.html

      . The Medical Subject Headings (MeSH) defines it as a decrease in skeletal muscle tone leading to decreased resistance to passive stretching

      National library of medicine. Pubmed [Internet]. Pubmed. 1977. Available from: https://www.ncbi.nlm.nih.gov/mesh/?term=muscle+hypotonia

      .
      However, some authors argue that the term is abstract, making it a diagnostic challenge
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      • Latash M.L.
      • Wood L.
      • Ulrich D.
      What is currently known about hypotonia, motor skill development, and physical activity in Down Syndrome.[Internet].
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , and advocate the need to create a scale that provides valid and reliable scores for its assessment
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      .
      Latash et al.
      • Latash M.L.
      • Zatsiorsky V.M.
      Muscle tone.
      claim that this may be due to the very imprecision in the definition of muscle tone, which is based on subjective terms, since resistance to stretching is a sensation that each evaluator may understand differently
      • Ganguly J.
      • Kulshreshtha D.
      • Almotiri M.
      • Jog M.
      Muscle tone physiology and abnormalities.
      .
      Muscle tone has been related to the monosynaptic stretch reflex, recognizing that it has a primordial role in the maintenance of posture, but also in the anticipation of movement, i.e., it acts not only in situations of relaxation, but also in moments of activity
      • Davidoff R.A.
      Skeletal muscle tone and the misunderstood stretch reflex.
      .
      Etiologically, the myotatic reflex, determined by the peripheral nervous system (PNS), is the main component of muscle tone, but the influence of central nervous system (CNS) structures is also defended: the basal ganglia or the red nucleus are structures that inhibit tone, and their lesion would create hypertonia
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      , and the cerebellum or striatum are facilitators of motor tone, and their lesion would give rise to hypotonia
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      . A mechanical component has also been described, determined by the contractile and damping capacity of the muscle fibers and the viscoelasticity of the protein of each muscle fiber
      • Ganguly J.
      • Kulshreshtha D.
      • Almotiri M.
      • Jog M.
      Muscle tone physiology and abnormalities.
      ,
      • Cameron-Tucker H.
      The neuropnysiology of tone : the role of the muscle spindle and the stretch reflex.
      ,
      • Pisano F.
      • Miscio G.
      • Colombo R.
      • Pinelli P.
      Quantitative evaluation of normal muscle tone.
      .
      The electromyogram (EMG) stands out as an objective test to assess muscle tone, but there is controversy as to the expected results. Masi et al.
      • Masi A.T.
      • Hannon J.C.
      Human resting muscle tone ( HRMT ): narrative introduction and modern concepts.
      stated that a silent EMG would be observed in the presence of normal passive muscle tone. However, Ganguly et al.
      • Ganguly J.
      • Kulshreshtha D.
      • Almotiri M.
      • Jog M.
      Muscle tone physiology and abnormalities.
      did not consider that the initial value of EMG could be equated to muscle tone, since EMG would detect motor unit activation, but cannot reveal the mechanical component, which is independent of neural activity.
      According to its origin, hypotonia can be classified as central and peripheral. Central hypotonia is associated with normal strength or mild to moderate weakness and antigravitational movements appear, although responses may be weaker. Peripheral hypotonia is associated with muscle weakness and absence of antigravity movements
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      .
      In this study, a systematic review (SR) is performed to find out what characteristics are described to be associated with hypotonia in children and what methods are used for its diagnosis.

      METHOD

      Sources of information and search strategy

      A literature review was performed following PRISMA recommendations
      • Moher D.
      • Shamseer L.
      • Clarke M.
      • et al.
      Preferred reporting items for systematic review and meta-analysis protocols ( PRISMA-P ) 2015 statement.
      to determine the characteristics associated with hypotonia and the tests described for its evaluation.
      The search for articles was performed in Pubmed/Medline, PEDro, Crochane, BVS, IBECS, MEDES, Web of Knowledge and Science Direct. Data were also collected from the Research Gate portal and Google Scholar. The references of the articles found were considered.
      The following MeSH terms were used for the search: "quantitative evaluation", "muscle tone", "symptom assesment", "floppy muscle", "muscle hypotonia", "infant" and "child". The Boolean AND / OR method was used, and the search was limited to articles where the terms were reflected in the title, abstract or keywords. We did not limit by publication date, to observe whether the concept of hypotonia, associated attributes and assessment methods, had become more clearly defined over time or whether the confusion observed by Naidoo in 2013
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      from 5 decades prior to conducting his study remains. The search was limited to articles in English and Spanish.

      Eligibility criteria and study selection.

      Inclusion criteria were articles describing characteristics associated with hypotonia or tests for the diagnosis or assessment of hypotonia.
      Exclusion criteria studies that exclusively analyzed peripheral hypotonia.
      The search and initial screening of titles and abstracts was performed independently by two reviewers. Duplicates and those articles that, after reading the title and abstract, did not clearly meet the inclusion criteria were eliminated.

      Data extraction and synthesis

      Both reviewers evaluated the articles and collected the data in a table, noting authors, date of publication, type of study, and the characteristics or evidence described. The quality of the studies was assessed using the guidelines recommended in EQUATOR: PEDro, STROBE, CASPE and CARE. The degree of evidence was evaluated according to the GRADE classification. Disagreements were resolved by the evaluation of a third reviewer.

      RESULTS

      Study selection

      A total of 8,778 articles were identified, of which 8,719 were in the different databases and 59 through other sources: reference lists, Research Gate and Google Scholar. Of the total, 3,652 were duplicates and were therefore eliminated. A reading of the titles and abstracts of the remaining 5,153 was performed, finding that 5,048 did not meet the eligibility criteria. A total of 105 studies were selected for full-text reading. Sixty of these did not describe attributes of hypotonia; some reported diseases associated with peripheral hypotonia exclusively or dealt with the diagnosis of diseases from a diagnosis of hypotonia without specifying the process. Others specified genetic tests to detect alterations compatible with hypotonia, but in no case did they mention the clinical characteristics of hypotonia or the tests that could be performed for its diagnosis.
      Finally, 45 studies were selected for analysis, with publication dates between 1982 and 2021 and written in three languages: English, Spanish and Danish (with an abstract in English), for which a translator was necessary.

      Characteristics of the studies

      Among the 45 articles identified, different types of studies were included. One was a randomized clinical trial (RCT)
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      ; three were case-control studies
      • De Santos-Moreno M.G.
      • Macias-Merlo M.L.
      • Gómez-Torrón A.
      Programas de bipedestación para la prevención de la displasia de cadera en niños con síndrome de Down [Standing programs for the prevention of hip dysplasia in children with Down syndrome].
      • Gontijo A.P.B.
      • Mancini M.C.
      • Silva P.L.
      • et al.
      Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait.

      De Santos-Moreno MG. Fisioterapia en Atención Temprana en niños con Síndrome de Down con patología respiratoria u otras alteraciones asociadas [Physiotherapy in Early Care in children with Down Syndrome with respiratory pathology or other associated alterations]. Beau Bassin: Editorial académica española; 2017. Spanish.

      ; two were case studies
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      ,
      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      , of which one analyzed a single case
      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      ; eleven were observational studies
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      ,
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      • Shuper A.
      • Weitz R.
      • Varsano I.
      • Mimouni M.
      Benign congenital hypotonia. A clinical study in 43 children.
      • Ghaffar H.A.
      • Elawady H.
      • Abouleinin I.
      • Rabie E.
      Diagnostic approach of floppy infants: a study in Fayoum University Hospital, Egypt. Middle East.
      • Paro-Panjan D.
      • Neubauer D.
      Congenital hypotonia: is there an algorithm?.
      • Vasta I.
      • Kinali M.
      • Messina S.
      • et al.
      Can clinical signs identifity newborns with neuromuscular disorders?.
      • Carboni P.
      • Pisani F.
      • Crescenzi A.
      • Villani C.
      Congenital hypotonia with favorable outcome.
      , four of which were surveys of professionals
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      ,
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      ; and twenty-eight were expert opinions, observational narrative descriptions, or literature reviews
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      ,
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      ,
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      ,
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      ,

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.

      Chu SY, Barlow SM. Capítulo1 A call for biomechanics to understand hypotonia and speech movement disorders in Down Syndrome. In: Advances in Communication disorders. Telangana. India: Avid Science Publications; 2016. p 2-40

      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      • Lenard H.G.
      Das >>Floppy infant<<.
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      • Prasad A.N.
      • Prasad C.
      The floppy infant: contribution of genetic and metabolic disorders.

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      • Christiansen S.
      • Miranda M.J.
      Algoritme til diagnosticering af slapt spædbarn [Algorithm for diagnosis of limp infant.
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      • Fahey M.
      Floppy baby.
      • Igarashi M.
      Floppy infant syndrome.
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      • Curran A.
      • Jardine E.
      The floppy infant.
      • Gaona V.A.
      Síndrome hipotónico del lactante [Hypotonic syndrome of the infant].
      • Larrivee D.
      Promise and possibility in the hypotonia infant.
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      . The articles presented hypotonia as an a priori diagnosis and its characteristics as confirmed facts.
      Levels of evidence for the studies, as proposed by the Oxford Centre for Evidence-Based Medicine (CEBM) are described as: Level 2 RCT; Level 2-3 observational and survey studies; Level 3-4 case-control studies; Level 4 case studies; and Level 5 studies based on expert opinion. Thus, of the 45 studies selected, 1 was level 2, 16 had a level between 2 and 4, and 28 articles were of very low quality, placing them at level 5.
      The articles were analyzed following the study presentation guidelines recommended in EQUATOR. The RCT
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      was reviewed with the PEDro scale, obtaining a score of 8/10; the observational studies
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      ,
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      • Shuper A.
      • Weitz R.
      • Varsano I.
      • Mimouni M.
      Benign congenital hypotonia. A clinical study in 43 children.
      • Ghaffar H.A.
      • Elawady H.
      • Abouleinin I.
      • Rabie E.
      Diagnostic approach of floppy infants: a study in Fayoum University Hospital, Egypt. Middle East.
      • Paro-Panjan D.
      • Neubauer D.
      Congenital hypotonia: is there an algorithm?.
      • Vasta I.
      • Kinali M.
      • Messina S.
      • et al.
      Can clinical signs identifity newborns with neuromuscular disorders?.
      • Carboni P.
      • Pisani F.
      • Crescenzi A.
      • Villani C.
      Congenital hypotonia with favorable outcome.
      with STROBE, obtaining 11 and 16 points out of 22; the studies developed by means of surveys
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      ,
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      with STROBE obtaining scores between 13 and 19; the case-control articles
      • De Santos-Moreno M.G.
      • Macias-Merlo M.L.
      • Gómez-Torrón A.
      Programas de bipedestación para la prevención de la displasia de cadera en niños con síndrome de Down [Standing programs for the prevention of hip dysplasia in children with Down syndrome].
      • Gontijo A.P.B.
      • Mancini M.C.
      • Silva P.L.
      • et al.
      Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait.

      De Santos-Moreno MG. Fisioterapia en Atención Temprana en niños con Síndrome de Down con patología respiratoria u otras alteraciones asociadas [Physiotherapy in Early Care in children with Down Syndrome with respiratory pathology or other associated alterations]. Beau Bassin: Editorial académica española; 2017. Spanish.

      with the CASPE guide specific for this type of research, obtaining 7 and 8 points out of 11; and the case studies
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      ,
      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      with the CARE guide, obtaining 10 and 15 out of a possible 30.
      The GRADE classification obtained a low or very low degree of evidence in 44 of the 45 studies. The only article with a higher grade of evidence, the RCT, supported its research on isokinetic work in children with Down syndrome (DS), assumed to be hypotonic, and the derived changes in strength and stability in these children after intervention, but the characteristics associated with hypotonia were described without the study aiming to confirm this relationship.
      Many of the studies described the characteristics associated with hypotonia, presenting them as a known and accepted relationship and naming them in the introduction itself
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      ,
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      ,
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      ,
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      ,
      • De Santos-Moreno M.G.
      • Macias-Merlo M.L.
      • Gómez-Torrón A.
      Programas de bipedestación para la prevención de la displasia de cadera en niños con síndrome de Down [Standing programs for the prevention of hip dysplasia in children with Down syndrome].
      ,

      De Santos-Moreno MG. Fisioterapia en Atención Temprana en niños con Síndrome de Down con patología respiratoria u otras alteraciones asociadas [Physiotherapy in Early Care in children with Down Syndrome with respiratory pathology or other associated alterations]. Beau Bassin: Editorial académica española; 2017. Spanish.

      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      ,
      • Ghaffar H.A.
      • Elawady H.
      • Abouleinin I.
      • Rabie E.
      Diagnostic approach of floppy infants: a study in Fayoum University Hospital, Egypt. Middle East.
      ,
      • Paro-Panjan D.
      • Neubauer D.
      Congenital hypotonia: is there an algorithm?.
      ,
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      ,
      • Lenard H.G.
      Das >>Floppy infant<<.
      ,
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      ,
      • Christiansen S.
      • Miranda M.J.
      Algoritme til diagnosticering af slapt spædbarn [Algorithm for diagnosis of limp infant.
      ,
      • Fahey M.
      Floppy baby.
      ,
      • Igarashi M.
      Floppy infant syndrome.
      ,
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      ,
      • Curran A.
      • Jardine E.
      The floppy infant.
      ,
      • Larrivee D.
      Promise and possibility in the hypotonia infant.
      ,
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      , and discussed other variables such as strength
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      ,
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      ; balance and stability
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      ; compensatory gait alterations
      • Gontijo A.P.B.
      • Mancini M.C.
      • Silva P.L.
      • et al.
      Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait.
      ; the presence of hip dysplasia
      • De Santos-Moreno M.G.
      • Macias-Merlo M.L.
      • Gómez-Torrón A.
      Programas de bipedestación para la prevención de la displasia de cadera en niños con síndrome de Down [Standing programs for the prevention of hip dysplasia in children with Down syndrome].
      ; alterations secondary to hypotonia in the respiratory tract

      De Santos-Moreno MG. Fisioterapia en Atención Temprana en niños con Síndrome de Down con patología respiratoria u otras alteraciones asociadas [Physiotherapy in Early Care in children with Down Syndrome with respiratory pathology or other associated alterations]. Beau Bassin: Editorial académica española; 2017. Spanish.

      ; developmental progression in children diagnosed with benign congenital hypotonia (BCH)
      • Shuper A.
      • Weitz R.
      • Varsano I.
      • Mimouni M.
      Benign congenital hypotonia. A clinical study in 43 children.
      ,
      • Paro-Panjan D.
      • Neubauer D.
      Congenital hypotonia: is there an algorithm?.
      ,
      • Carboni P.
      • Pisani F.
      • Crescenzi A.
      • Villani C.
      Congenital hypotonia with favorable outcome.
      ; or classification as central or peripheral hypotonia
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      ,
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      ,
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      ,
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      ,
      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      ,
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      ,

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      ,
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      ,

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      • Christiansen S.
      • Miranda M.J.
      Algoritme til diagnosticering af slapt spædbarn [Algorithm for diagnosis of limp infant.
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      ,
      • Igarashi M.
      Floppy infant syndrome.
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      ,
      • Gaona V.A.
      Síndrome hipotónico del lactante [Hypotonic syndrome of the infant].
      ,
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      . The articles that referred to clinical assessment tests for hypotonia described assessment maneuvers, sometimes presented as commonly used
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      ,
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      ,

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      ,, but without providing the validity or reliability of these tests.
      The only articles that attempted to determine how to measure hypotonia or to define what characteristics were consensually associated were those developed using surveys
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      ,
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      .

      Tests and characteristics associated with hypotonia

      Fifty-three characteristics or assessment tests associated with infantile hypotonia were identified. Variability was observed in terms of the aspect on which they impacted, describing alterations in cognitive, imitative, and social skills, age of acquisition of motor milestones, musculoskeletal apparatus, suspension and balance reactions, posture and coordination in movement, and oromotor, respiratory or digestive dysfunctions.
      Martin et al.
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      in their survey studies, asked practitioners to provide methods used for the assessment of hypotonia and found that 73% of therapists did not use any formal instruments and, among those who reported the use of assessment methods, observation was the most cited system, which, along with joint range of motion, was mentioned by 20.5%.
      Naidoo et al.
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      conducted a study with physicians (pediatricians and neuropediatricians) and therapists (occupational therapists and physical therapists) and collected responses on the methods used to diagnose hypotonia and, again, observation was the most prominent. In addition, 70% of respondents noted the subjectivity of the diagnosis and 78% the complexity of its quantification. The author highlighted the lack of agreement between the observations made by the different professional disciplines.
      In terms of frequency, the pull-to-sit test, which assesses the drooping of the head when the child is pulled with the hands to move from the supine to the sitting position, was the most frequently mentioned, appearing in 25 of the 45 studies. In 22 studies the frog posture was described when the child was relaxed in the supine position, and in 21 the vertical suspension with the sensation of the child slipping between the hands. Between 15 and 20 times appeared the association with hypermobile joints and ventral suspension in which the hypotonic child could not stay in the horizontal line. The scarf sign, which consists of bringing the child's hand to the opposite shoulder and observing the position reached by the elbow with respect to the sternum, was mentioned 14 times, as well as the difficulty in maintaining antigravitational postures. The sensation of less resistance when passively mobilizing a joint was raised in 12 studies, alterations in respiratory patterns in 11, and in 10 reference was made to alterations in feeding patterns and the presence of inadequate body postures. The rest of the characteristics were collected on fewer occasions.
      The articles classified hypotonia, according to its origin, as central or peripheral, assigning different attributes in each case
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      ,
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      ,
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      ,
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      ,
      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      ,
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      ,

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      ,
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      ,
      • Prasad A.N.
      • Prasad C.
      The floppy infant: contribution of genetic and metabolic disorders.
      ,

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      ,
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      ,
      • Igarashi M.
      Floppy infant syndrome.
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      ,
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      ,
      • Gaona V.A.
      Síndrome hipotónico del lactante [Hypotonic syndrome of the infant].
      ,
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      and described syndromes related to each etiology
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      ,

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      ,
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      • Prasad A.N.
      • Prasad C.
      The floppy infant: contribution of genetic and metabolic disorders.

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      ,
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      ,
      • Igarashi M.
      Floppy infant syndrome.
      ,
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      ,
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      • Curran A.
      • Jardine E.
      The floppy infant.
      • Gaona V.A.
      Síndrome hipotónico del lactante [Hypotonic syndrome of the infant].
      ,
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      . Kaur et al.
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      stated that 60-80% of hypotonia cases were of central origin.

      DISCUSSION

      According to the data derived from this SR, a low and very low quality of studies on hypotonia has been observed, confirming the need to find a consensus regarding the motor tone and hypotonia definitions. Only in this way will it be possible to analyze precisely which characteristics are reliably related to this attribute, to carry out research work that confirms these data and to be able to support them with scientific evidence. The imprecision and confusion denounced by Naidoo in 2013
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      is therefore maintained.
      Responding to the objective of knowing what characteristics are described as associated with hypotonia in children and what methods are used for its diagnosis, a variety of attributes have been found, some of them controversial, especially on strength, differentiation with hypermobility and the ability to maintain postures against gravity.
      When referring to muscle strength, several authors accept it as a differential characteristic between central and peripheral hypotonia
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      ,
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      ,
      • Vasta I.
      • Kinali M.
      • Messina S.
      • et al.
      Can clinical signs identifity newborns with neuromuscular disorders?.
      ,
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      ,

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , considering that it is maintained at values close to normal in the case of central origin

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , and weakness would be observed in the case of peripheral involvement. With the aim of finding out the relationship between strength and hypotonia, research was carried out measuring strength in children affected by syndromes described with the presence of central hypotonia. Reus et al.
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      carried out a study in which they compared the strength of an experimental group (EG) formed by children with Prader Willi Syndrome (PWS) and that of a control group (CG) of children with typical development, and observed that the EG presented, in general, lower muscle strength than the CG and that, in those children of the EG in whom a greater decrease in strength was evidenced, this was associated with a delay in the acquisition of motor milestones. On the other side, in the CG, which presented greater muscle strength, children who excelled more in this attribute were not related to having a greater acquisition of milestones.
      Martin et al.
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      developed two studies using surveys sent to occupational therapists (OT) and physical therapists (PT), in order to identify the characteristics they detected in children that they understood to be related to hypotonia. In both studies it was found that decreased muscle strength was among the most named characteristics, as also occurred in the literature review conducted by Naidoo
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      who identified attributes related to hypotonia and where muscle strength was present among the 11 selected characteristics. In the RCT developed by Eid et al.
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      with people with DS, they observed a decrease in strength in addition to difficulty in maintaining antigravitational postures. Therefore, although it is understood that in central hypotonia muscle strength is close to normal
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , and the importance of differentiating between weakness and hypotonia is defended
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      ,
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , strength is included as one of the most frequent alterations that manifest from hypotonia and is analyzed and admitted in syndromes derived from a central alteration such as DS or PWS.
      Regarding hypermobility, Carboni et al.
      • Carboni P.
      • Pisani F.
      • Crescenzi A.
      • Villani C.
      Congenital hypotonia with favorable outcome.
      analyzed whether there was an association between both variables in a group of 41 children who had been diagnosed with BCH and obtained results, although they did not provide statistical data except percentages, which indicated the correlation between both characteristics and even suggested that children with BCH, in their adult life, will present joint hyperlaxity. Paro-Pajan et al.
      • Paro-Panjan D.
      • Neubauer D.
      Congenital hypotonia: is there an algorithm?.
      also developed their research on BCH, which they did not consider a disease but a clinical sign, with the aim of creating an algorithm that would lead them, from the diagnosis of hypotonia, to know the etiological diagnosis. Hypotonia was decided based on observation of the child and the presence of hyperextensible joints.
      Strength is developed by the contractile capacity of muscle fibers, hypermobility is determined by the elongation of a ligament or the capacity of tissues, such as the joint capsule, to maintain joint congruency. If we accept a mechanical component in tone, determined by the quality of the soft tissues and their viscoelasticity, it can be understood that ligamentous tissues can also be affected in the presence of hypotonia, presenting clinical hypermobility.
      The third characteristic contributed in the study by Martin et al.
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      was the difficulty in maintaining antigravitational postures. This characteristic is also marked in the consensus study by Naidoo et al.
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      in which they identified 24 characteristics associated with hypotonia that were agreed upon by 11 experts from different areas, pediatricians, neuropediatricians, OT and PT, obtaining the greatest consensus in the presence of abnormal postures and the limitation to acquire or prolong an antigravitational posture over time. Shuper et al.
      • Shuper A.
      • Weitz R.
      • Varsano I.
      • Mimouni M.
      Benign congenital hypotonia. A clinical study in 43 children.
      conducted a study with a sample of 43 children diagnosed with BCH by observation. They observed that, when performing the vertical suspension maneuver, the children presented the sitting posture in the air. Furthermore, they concluded that they could not state whether it was a central or peripheral hypotonia. This sitting-in-air posture develops against gravity, which would be incongruent with the previous statements since, in the case of peripheral hypotonia, antigravity postures would be absent and in the case of central hypotonia they would be weaker responses when provoked, but this group of children performed the sitting-in-air posture without being a necessity or expected response.
      Other authors
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      ,

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      , considered 4 maneuvers of choice for the diagnosis of hypotonia in children: the pull to sit test, the scarf sign, vertical suspension and horizontal suspension, although in the review we have not located any study demonstrating their validity or reliability. The horizontal suspension was observed as one of the most commonly used tests to assess hypotonia, including that of central origin, and its response depends on the maintenance of the posture against gravity, which would imply that there is a difficulty in the acquisition of these postures.
      Soucy et al.
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      in their study on methods of assessment and diagnosis of hypotonia, with a sample of 55 children with Neurofibromatosis type 1, proposed that the most predictive measurement of hypotonia consisted of two tests: the hip abduction range and the pull-to-sit test. They observed that children who had an abduction angle greater than 60° and had a greater head drop were 20 times more likely to have hypotonia.
      The variability between the authors' proposals is maintained in different studies. Thus, Mesquita et al.
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      supported the use of the section for the evaluation of tone in the neonatal neurological examination (HNNE), which includes the scarf sign, popliteal angle, ankle dorsiflexion angle and vertical suspension; Moore et al.
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      indicated that the frog posture, scarf sign, joint hyperextensibility, and pull-to-sit test were the most representative tests of hypotonia, but they also added that there were scales that assessed hypotonia, naming among them the Peabody scale (PDMS), the Bayley Scale for Infant Development, the Denver Developmental Scale, the Hawaii Early Learning Profile (HELP), and the INFANIB checklist, all of which are either screening tests to detect children at psychomotor risk or scales to assess the child's motor or global development. None of these scales, except the INFANIB, mentions or is considered to measure motor tone, so it can be understood that they were establishing a direct relationship between motor development and hypotonia without any scientific basis to support it.
      Of all the scales described, only the INFANIB and HNNE describe tests that assess tone, including tests based on antigravity positions such as ventral suspension. These scales are administered to children to assess central hypotonia.
      From the results of this SR, there is a variety of opinions regarding the tests to be performed for the diagnosis of hypotonia and a diagnostic difficulty, without reliable and valid methods for it, and subjective, based mainly on observation
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      ,
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      . Of the methods described by Naidoo et al.
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      ,
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      for its evaluation, only the development of milestones can be measured and their relationship to hypotonia is not confirmed. The lack of consensus makes understanding between the different professionals difficult and, therefore, makes the information to the family more complex, making it difficult to understand the development of their child.
      Finally, regarding the variability of motor tone, while some authors defend that motor tone is not modified, but is a characteristic of the individual, others describe an improvement in tone after receiving therapeutic interventions, confirming this improvement in the motor development scales, or measuring strength. Therapists who participated in the surveys conducted by Martin et al.
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      ,
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      responded to the question on tone variability and 85.4% reported that tone improved with therapy, basing this statement on the observed increase in strength, acquisition of motor milestones and increase in endurance.
      Once again, the equating of motor development and strength with tone is observed, although the literature advocates the need to differentiate these concepts
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      .
      Muscle tone is determined by the viscoelasticity of muscle proteins, with a contraction command issued by the PNS via the myotatic reflex and supervised by the CNS. Accepting this, it seems complex to demonstrate that a therapeutic intervention can act on any of these components, but it may be that, by promoting muscle work, hypertrophy of the tissue is produced, and this allows greater development of strength, but the greatest trophism will be obtained with the quality of a hypotonic muscle.

      Limitations

      The main limitation could correspond to the loss of studies due to the search performed, either because of the choice of the terms selected or because of the databases chosen.
      Another issue has been the low quality of the studies identified and the scarce scientific evidence they present in general, which highlights the need for research in this area.
      Furthermore, the large number of associated characteristics and the lack of a clear and consensual definition do not ensure that different authors are reporting the same hypotonia condition, and therefore, that we are relating different concepts.

      CONCLUSIONS

      According to the data collected in this systematic review, there is a wide variety of characteristics associated with hypotonia, some of them highly debated without reaching a consensus, such as muscle strength, hypermobility or the maintenance of antigravity postures.
      Inconsistencies are observed regarding the alterations that hypotonia may present according to its origin, central or peripheral.
      The most used test in the diagnosis of hypotonia is observation, followed by the pull-to-sit test, the adoption of the frog posture, vertical suspension, horizontal suspension, and the scarf sign.
      No test or scale has been found to produce valid and reliable scores for the diagnosis and quantification of hypotonia.
      The quality of the studies included in this systematic review is low and they are mostly expert opinions.
      Figure thumbnail gr1
      figure 1PRISMA flow diagram demonstrating the screening process for this review.
      Figure thumbnail gr2
      figure 2Characteristics associated with hypotonia. Frequency graph.
      Table 1Search strategy and identified studies
      DatabaseMesh termsBoolean OperatorsNumber of identified studiesTotal
      PUBMEDMuscle hypotonia

      Children

      Quantitative evaluation
      AND/OR3311152
      Floppy muscle

      Infant
      AND328
      Muscle tone

      Children

      Symptom assessment
      AND/OR493
      PEDroQuantitative evaluation

      Muscle tone
      AND/OR1719
      Floppy muscle

      Infant
      AND0
      Muscle hypotonia

      Children
      AND/OR2
      COCHRANEQuantitative evaluation

      Muscle tone
      AND6081006
      Floppy muscle

      Infant
      AND145
      Muscle hypotonia

      Children
      AND253
      BVSMuscle hypotonia

      Children

      Quantitative evaluation
      AND1782021
      Floppy muscle

      Infant
      AND1843
      Muscle tone

      Children

      Symptom assessment
      AND0
      MEDESQuantitative evaluation

      Muscle tone
      AND921
      Floppy muscle

      Infant
      AND0
      Muscle hypotonia

      Children
      AND12
      Web of scienceQuantitative evaluation

      Muscle tone
      AND14371443
      Floppy muscle

      Infant
      AND3
      Muscle hypotonia

      Children
      AND3
      Science directQuantitative evaluation

      Muscle tone

      Children

      Hypotonia
      AND30573057
      Table 2Included studies
      StudyCountryStudy typeQualityCharacteristics
      Martin et al. (2005)
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      EEUUSurveys to professionalsSTROBE 13/22Decreased strength

      Decreased task tolerance

      Scarf sign

      Poor antigravity posture

      Rounded shoulders

      Leaning on to supports

      Exaggerated hip abduction
      Diminished resistance to passive movement

      Popliteal angle

      Hypermobile joints

      Increased flexibility

      Poor attention or motivation

      Delayed motor skills
      Hartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      Expert opinionWeakness

      Pull to sit

      Vertical suspension

      Horizontal suspension

      Lack of posture regulation
      Frog-like posture

      Poor state of alertness

      Delayed motor skills

      Amimia
      Naidoo (2013)
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      South AfricaSurveys to professionalsSTROBE 15/22Decreased task tolerance

      Hypermobile joints

      Frog-like posture

      W sitting

      Increased flexibility
      Leaning on to supports

      Delayed motor skills

      Diminished resistance to passive movement

      Winging of the scapula posture
      Bodensteiner (2008)
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      Expert opinionPull to sit

      Scarf sign
      Vertical suspension

      Horizontal suspension
      Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      Expert opinionPull to sit

      Vertical suspension

      Horizontal suspension

      Poor trunk extension

      Astasia

      Wide-based gait

      Lack of posture regulation

      Genu recurvatum

      Exaggerated hip abduction

      Hypermobile joints

      Gastroesophageal reflux

      Frog-like posture
      Diminished resistance to passive movement

      Lack of response to environmental stimuli

      Plagiocephaly

      W sitting

      Exaggerated ankle dorsiflexion

      Hyperpronation of the feet

      Delayed motor skills

      Irregular breathing patterns

      Swallowing problems

      Oral-motor dysfunction

      Amimia

      Poor state of alertness
      Madhok et al. (2021)

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      Expert opinionPull to sit

      Scarf sign

      Irregular breathing patterns
      Vertical suspension

      Horizontal suspension
      Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      NetherlandsObservational study

      N=81TDe+17PWS

      Strength measurement
      STROBE 16/22Pull to sit

      Scarf sign

      Vertical suspension

      Horizontal suspension

      Frog-like posture
      Diminished resistance to passive movement

      Poor antigravity posture

      Hypermobile joints

      Delayed motor skills
      Martin et al. (2007)
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      EEUUSurveys to professionalsSTROBE 15/22Decreased strength

      Poor endurance

      Decreased task tolerance

      Palpation

      Abnormal postures

      Increased flexibility
      Poor antigravity posture

      Rounded shoulders

      Leaning on to supports

      Hypermobile joints

      Poor attention or motivation

      Delayed motor skills
      Harris (2008)
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      Expert opinionSlow responses

      Weakness

      Pull to sit
      Poor antigravity posture

      Delayed motor skills
      Prats-Viñas (2008)
      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      Expert opinionPull to sit

      Horizontal suspension

      Palpation
      Amimia

      Constipation

      Irregular breathing patterns
      De Santos-Moreno et al. (2017)
      • De Santos-Moreno M.G.
      • Macias-Merlo M.L.
      • Gómez-Torrón A.
      Programas de bipedestación para la prevención de la displasia de cadera en niños con síndrome de Down [Standing programs for the prevention of hip dysplasia in children with Down syndrome].
      SpainCase-control

      N=76 DS

      Hip dysplasia
      CASPE 7/11W sitting

      Genu recurvatum
      Hypermobile joints

      Hip dysplasia
      Soucy et al. (2015)
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      EEUUCase study

      N=55 children with Neurofibromatosis type 1.

      Assess hypotonia
      CARE 15/30Decreased strength

      Pull to sit

      Triceps fat percentage

      Hypermobile joints
      Exaggerated ankle dorsiflexion

      Genu recurvatum

      Exaggerated hip abduction
      Dipak et al. (2019)
      • Dipak N.K.
      • Pandya S.
      • Hajirnis O.
      • Munde B.P.
      Floppy neonate with feeding difficulties.
      IndiaSingle case.

      SPW
      CARE

      10/30
      Swallowing problems

      High arched palate
      Weak cry
      Gowda et al. (2007)
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      Expert opinionPull to sit

      Frog-like posture

      Poor antigravity posture

      Fisted hands
      Diminished resistance to passive movement

      Hypermobile joints

      Delayed motor skills
      Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      South AfricaSurveys to professionalsSTROBE 19/22Poor endurance

      Decreased task tolerance

      Rag-doll posture

      Weakness

      Palpation

      Reduced balance

      Abnormal postures

      Frog-like posture

      W sitting

      Amimia
      Leaning on to supports

      Asymmetry or postural fixations

      Hyperpronation of the feet

      Hypermobile joints

      Increased flexibility

      Delayed motor skills

      Excessive drooling

      Winging of the scapula posture

      Diminished resistance to passive movement
      Mesquita et al. (2018)
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      PortugalObservational study

      N=91 infants diagnosed with hypotonia.

      Assess diagnostic accuracy over time.
      STROBE 14/22Scarf sign

      Vertical suspension

      Horizontal suspension

      Weakness
      Poor state of alertness

      Fisted hands Popliteal angle

      Exaggerated ankle dorsiflexion
      Lenard (1982)
      • Lenard H.G.
      Das >>Floppy infant<<.
      Expert opinionRag-doll posture

      Vertical suspension

      Horizontal suspension
      Diminished resistance to passive movement Hypermobile joints
      Carboni et al. (2002)
      • Carboni P.
      • Pisani F.
      • Crescenzi A.
      • Villani C.
      Congenital hypotonia with favorable outcome.
      ItalyObservational study

      Follow-up BCH
      STROBE 11/22W sitting

      Hyperpronation of the feet
      Asymmetry or postural fixations

      Winging of the scapula posture
      Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      Expert opinionWeakness

      Pull to sit

      Vertical suspension

      Horizontal suspension

      Abnormal postures

      Lack of posture regulation

      Frog-like posture

      Poor antigravity posture

      Weak cry

      Fisted hands

      Hypermobile joints
      Diminished resistance to passive movement

      Lack of response to environmental stimuli

      Decreased of spontaneous movements

      Delayed motor skills

      Poor state of alertness

      Irregular breathing patterns

      Inability to cough

      Swallowing problems

      Oral-motor dysfunction

      Amimia
      Eid et al. (2017)
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      Saudi ArabiaRCT

      EG=15DS; CG=16DS

      Measures stability and strength with isokinetic treatment
      PEDro

      8/10
      Decreased strength

      Reduced balance

      Delayed motor skills
      Abnormal postures

      Poor antigravity posture

      Weakness
      Chu et al. (2016)

      Chu SY, Barlow SM. Capítulo1 A call for biomechanics to understand hypotonia and speech movement disorders in Down Syndrome. In: Advances in Communication disorders. Telangana. India: Avid Science Publications; 2016. p 2-40

      Expert opinionPoor endurance

      Amimia
      Diminished resistance to passive movement

      Oral-motor dysfunction
      Gontijo et al. (2008)
      • Gontijo A.P.B.
      • Mancini M.C.
      • Silva P.L.
      • et al.
      Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait.
      BrazilCase-control

      EG=12DS; CG=12TDe

      Gait analysis
      CASPE

      7/11
      Poor endurancePalpation
      Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      Expert opinionPull to sit

      Vertical suspension

      Horizontal suspension

      Abnormal postures

      Frog-like posture

      Poor antigravity posture

      Weak cry

      Hypermobile joints

      Excessive drooling
      Diminished resistance to passive movement

      Decreased of spontaneous movements

      Poor state of alertness

      Irregular breathing patterns

      Inability to cough

      Swallowing problems

      Oral-motor dysfunction

      Amimia
      Mercuri et al. (2019)
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      Expert opinionRag-doll posture

      Scarf sign

      Horizontal suspension
      Popliteal angle

      Irregular breathing patterns

      Swallowing problems
      De Santos-Moreno (2017)

      De Santos-Moreno MG. Fisioterapia en Atención Temprana en niños con Síndrome de Down con patología respiratoria u otras alteraciones asociadas [Physiotherapy in Early Care in children with Down Syndrome with respiratory pathology or other associated alterations]. Beau Bassin: Editorial académica española; 2017. Spanish.

      SpainCase-control

      N=67DS.

      Respiratory pathology
      CASPE

      8/11
      Irregular breathing patterns

      Swallowing problems

      Protruding tongue
      Gastroesophageal reflux

      Recurrent respiratory infections
      Gaona (2013)
      • Gaona V.A.
      Síndrome hipotónico del lactante [Hypotonic syndrome of the infant].
      Expert opinionVertical suspension

      Fisted hands
      Delayed motor skills
      Sparks (2015) Expert opinionPull to sit

      Scarf sign
      Vertical suspension

      Horizontal suspension
      Kaler et al. (2020)
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      Expert opinionWeakness

      Pull to sit

      Vertical suspension

      Frog-like posture

      Fisted hands
      Amimia

      Hypermobile joints

      Delayed motor skills

      Poor state of alertness
      Prasad et al. (2003)
      • Prasad A.N.
      • Prasad C.
      The floppy infant: contribution of genetic and metabolic disorders.
      Expert opinionWeakness

      Pull to sit

      Frog-like posture
      Amimia

      Poor antigravity posture
      Jain et al. (2011)
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      Expert opinionPull to sit

      Vertical suspension

      Horizontal suspension

      Frog-like posture

      Poor antigravity posture

      Plagiocephaly

      Hip dysplasia

      Hypermobile joints
      Diminished resistance to passive movement

      Fisted hands

      Asymmetry or postural fixations

      Delayed motor skills

      Lack of response to environmental stimuli

      Irregular breathing patterns

      Swallowing problems
      Sender et al. (2003)
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      Expert opinionPull to sit

      Scarf sign

      Vertical suspension

      Horizontal suspension
      Frog-like posture

      Hip dysplasia

      Popliteal angle
      Igarashi (2004)
      • Igarashi M.
      Floppy infant syndrome.
      Expert opinionPull to sit

      Scarf sign

      Vertical suspension

      Horizontal suspension

      Abnormal postures

      Delayed motor skills
      Frog-like posture

      Rounded shoulders

      Exaggerated ankle dorsiflexion

      Hypermobile joints

      Increased flexibility
      Bay (2006)

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      Expert opinionPull to sit

      Scarf sign

      Vertical suspension

      Horizontal suspension

      Hypermobile joints

      Delayed motor skills

      Swallowing problems

      Oral-motor dysfunction
      Abnormal postures

      Frog-like posture

      Asymmetry or postural fixations

      Exaggerated hip abduction

      Irregular breathing patterns

      Recurrent respiratory infections

      Excessive drooling
      Christiansen et al. (2015)
      • Christiansen S.
      • Miranda M.J.
      Algoritme til diagnosticering af slapt spædbarn [Algorithm for diagnosis of limp infant.
      Expert opinionPull to sit

      Vertical suspension
      Frog-like posture
      Moore et al. (2000)
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      Expert opinionPull to sit

      Scarf sign
      Frog-like posture

      Hypermobile joints
      Reed (2007)
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      Expert opinionPull to sit

      Scarf sign

      Delayed motor skills
      Horizontal suspension

      Frog-like posture
      Fahey (2015)
      • Fahey M.
      Floppy baby.
      Expert opinionPull to sit

      Scarf sign

      Vertical suspension
      Abnormal postures

      Frog-like posture

      Asymmetry or postural fixations
      Prasad et al. (2011)
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      Expert opinionPull to sit

      Scarf sign

      Vertical suspension

      Horizontal suspension
      Abnormal postures

      Frog-like posture

      Irregular breathing patterns

      Swallowing problems
      Tirado-Pérez et al. (2018)
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      Expert opinionPull to sit

      Vertical suspension

      Horizontal suspension
      Frog-like posture

      Poor antigravity posture

      Delayed motor skills
      Curran et al. (1998)
      • Curran A.
      • Jardine E.
      The floppy infant.
      Expert opinionPull to sit

      Frog-like posture
      Irregular breathing patterns
      Shuper et al. (1987)
      • Shuper A.
      • Weitz R.
      • Varsano I.
      • Mimouni M.
      Benign congenital hypotonia. A clinical study in 43 children.
      IsraelObservational study

      N=43

      Follow-up BCH
      STROBE 11/22Vertical suspensionDelayed motor skills
      Ghaffar et al. (2017)
      • Ghaffar H.A.
      • Elawady H.
      • Abouleinin I.
      • Rabie E.
      Diagnostic approach of floppy infants: a study in Fayoum University Hospital, Egypt. Middle East.
      EgyptObservational studySTROBE 16/22Hypermobile joints

      Abnormal postures
      Diminished resistance to passive movement

      Delayed motor skills
      Larrive (2019)
      • Larrivee D.
      Promise and possibility in the hypotonia infant.
      Expert opinionFrog-like posture

      Poor antigravity posture
      Hypermobile joints
      Paro-Panjan et al. (2004)
      • Paro-Panjan D.
      • Neubauer D.
      Congenital hypotonia: is there an algorithm?.
      SloveniaObservational study

      N=134

      Follow-up of newborn with BCH
      STROBE 13/22Poor antigravity postureLack of response to environmental stimuli
      Vasta et al. (2005)
      • Vasta I.
      • Kinali M.
      • Messina S.
      • et al.
      Can clinical signs identifity newborns with neuromuscular disorders?.
      United KingdomObservational study

      N=83

      Follow-up of newborn with hypotonia and weakness
      STROBE 14/22Poor antigravity posture

      Irregular breathing patterns
      Swallowing problems
      Table 3Tests and characteristics associated with hypotonia and studies that provide them.
      CharacteristicsStudies
      Decreased strengthMartin et al. (2005)
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      , Martin et al. (2007)
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      , Soucy et al. (2015)
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      , Eid et al. (2017)
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      Poor enduranceMartin et al. (2007)
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      , Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      , Chu et al. (2016)

      Chu SY, Barlow SM. Capítulo1 A call for biomechanics to understand hypotonia and speech movement disorders in Down Syndrome. In: Advances in Communication disorders. Telangana. India: Avid Science Publications; 2016. p 2-40

      , Gontijo et al. (2008)
      • Gontijo A.P.B.
      • Mancini M.C.
      • Silva P.L.
      • et al.
      Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait.
      Decreased of spontaneous movementsKaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      Decreased task toleranceMartin et al. (2005)
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      , Naidoo (2013)
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      , Martin et al. (2007)
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      , Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      Slow responsesHarris (2008)
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      Rag-doll postureNaidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      , Lenard (1982)
      • Lenard H.G.
      Das >>Floppy infant<<.
      , Mercuri et al. (2019)
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      Weakness, especially axialHartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      , Harris (2008)
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      , Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Eid et al. (2017)
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      , Mesquita et al. (2018)
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      , Kaler et al. (2020)
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      , Prasad et al. (2003)
      • Prasad A.N.
      • Prasad C.
      The floppy infant: contribution of genetic and metabolic disorders.
      Pull to sitHartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      , Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , Madhok et al. (2021)

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      , Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      , Bodensteiner (2008)
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      , Harris (2008)
      • Harris S.R.
      Congenital hypotonia: clinical and developmental assessment.
      , Prats-Viñas (2008)
      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      , Prasad et al. (2011)
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      , Soucy et al. (2015)
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      , Gowda et al. (2007)
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      , Kaler et al. (2020)
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      , Prasad et al. (2003)
      • Prasad A.N.
      • Prasad C.
      The floppy infant: contribution of genetic and metabolic disorders.
      , Jain et al. (2011)
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Bay (2006)

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , Christiansen et al. (2015)
      • Christiansen S.
      • Miranda M.J.
      Algoritme til diagnosticering af slapt spædbarn [Algorithm for diagnosis of limp infant.
      , Sender et al. (2003)
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Fahey (2015)
      • Fahey M.
      Floppy baby.
      , Igarashi (2004)
      • Igarashi M.
      Floppy infant syndrome.
      , Tirado-Pérez et al. (2018)
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      , Sparks (2015), Moore et al. (2000)
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      , Reed (2007)
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      , Curran et al. (1998)
      • Curran A.
      • Jardine E.
      The floppy infant.
      Scarf signMartin et al..(2005)
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      , Madhok et al. (2021)

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      , Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      , Bodensteiner (2008)
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      , Prasad et al. (2011)
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      , Mesquita et al. (2018)
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      , Mercuri et al. (2019)
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      , Bay (2006)

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , Sender et al. (2003)
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Fahey (2015)
      • Fahey M.
      Floppy baby.
      , Igarashi (2004)
      • Igarashi M.
      Floppy infant syndrome.
      , Sparks (2015), Moore et al. (2000)
      • Moore D.P.
      • Kowalske K.J.
      Neuromuscular rehabilitation and electrodiagnosis. 5. Myopathy.
      , Reed (2007)
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      Triceps fat percentageSoucy et al. (2015)
      • Soucy E.A.
      • Wessel L.E.
      • Gao F.
      • Albers A.C.
      • Gutmann D.H.
      • Dunn C.M.
      A pilot study for evaluation of hypotonia in children with neurofibromatosis type 1.
      PalpationMartin et al. (2007)
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      , Prats-Viñas (2008)
      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      , Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      ,Gontijo et al. (2008)
      • Gontijo A.P.B.
      • Mancini M.C.
      • Silva P.L.
      • et al.
      Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait.
      Vertical suspensionHartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      , Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , Madhok et al. (2021)

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      , Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      , Bodensteiner (2008)
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      , Prasad et al. (2011)
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      , Mesquita et al. (2018)
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      , Lenard (1982)
      • Lenard H.G.
      Das >>Floppy infant<<.
      , Kaler et al. (2020)
      • Kaler J.
      • Hussain A.
      • Patel S.
      • Majhi S.
      Neuromuscular junction disorders and floppy infant syndrome: a comprehensive review.
      , Jain et al. (2011)
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Bay (2006)

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , Christiansen et al. (2015)
      • Christiansen S.
      • Miranda M.J.
      Algoritme til diagnosticering af slapt spædbarn [Algorithm for diagnosis of limp infant.
      , Sender et al. (2003)
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Fahey (2015)
      • Fahey M.
      Floppy baby.
      , Igarashi (2004)
      • Igarashi M.
      Floppy infant syndrome.
      , Tirado-Pérez et al. (2018)
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      , Sparks (2015), Shuper et al. (1987)
      • Shuper A.
      • Weitz R.
      • Varsano I.
      • Mimouni M.
      Benign congenital hypotonia. A clinical study in 43 children.
      , Gaona (2013)
      • Gaona V.A.
      Síndrome hipotónico del lactante [Hypotonic syndrome of the infant].
      Horizontal suspensionHartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      , Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , Madhok et al. (2021)

      Madhok SS, Shabbir N. Hypotonia [Internet]. StatPearls. 2021 [cited 2021 May 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32965880

      , Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      , Bodensteiner (2008)
      • Bodensteiner J.B.
      The evaluation of the hypotonic infant.
      , Prats-Viñas (2008)
      • Prats-Viñas J.M.
      Enfoque diagnóstico del niño hipotónico [Diagnostic approach to the hypotonic child]. Protocolos diagnósticos en Neurología pediátrica [Internet].
      , Prasad et al. (2011)
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      , Mesquita et al. (2018)
      • Mesquita M.
      • Ratola A.
      • Tiago J.
      • Basto L.
      Neonatal hypotonia: is it a diagnostic challenge?.
      , Lenard (1982)
      • Lenard H.G.
      Das >>Floppy infant<<.
      , Mercuri et al. (2019)
      • Mercuri E.
      • Pera M.C.
      • Brogna C.
      Neonatal hypotonia and neuromuscular conditions.
      , Jain et al. (2011)
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Bay (2006)

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , Sender et al. (2003)
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Igarashi (2004)
      • Igarashi M.
      Floppy infant syndrome.
      , Tirado-Pérez et al. (2018)
      • Tirado-Pérez I.S.
      • Zarate-Vergara A.C.
      Initial approach hypotonic syndrome “Floppy infant.
      , Sparks (2015), Reed (2007)
      • Reed U.C.
      Síndrome del niño hipotónico: causas neuromusculares [Hypotonic infant syndrome: neuromuscular causes].
      Diminished resistance to passive movementMartin et al. (2005)
      • Martin K.
      • Inman J.
      • Kirschner A.
      • Deming K.
      • Gumbel R.
      • Voelker L.
      Characteristics of hypotonia in children: A consensus opinion of pediatric occupational and physical therapists.
      , Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , Naidoo (2013)
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      , Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.
      , Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      , Gowda et al. (2007)
      • Gowda V.
      • Parr J.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Chu et al. (2016)

      Chu SY, Barlow SM. Capítulo1 A call for biomechanics to understand hypotonia and speech movement disorders in Down Syndrome. In: Advances in Communication disorders. Telangana. India: Avid Science Publications; 2016. p 2-40

      , Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      , Lenard (1982)
      • Lenard H.G.
      Das >>Floppy infant<<.
      , Jain et al. (2011)
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Ghaffar et al. (2017)
      • Ghaffar H.A.
      • Elawady H.
      • Abouleinin I.
      • Rabie E.
      Diagnostic approach of floppy infants: a study in Fayoum University Hospital, Egypt. Middle East.
      Reduced balanceNaidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      , Eid et al. (2017)
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      Abnormal posturesMartin et al. (2007)
      • Martin K.S.
      • Kaltenmark T.
      • Lewallen A.
      • Smith C.
      • Yoshida A.
      Clinical characteristics of hypotonia: a survey of pediatric physical and occupational therapists.
      , Prasad et al. (2011)
      • Prasad A.N.
      • Prasad C.
      Genetic evaluation of the floppy infant.
      , Naidoo et al. (2013)
      • Naidoo P.
      • Joubert R.W.
      Consensus on hypotonia via Delphi process.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      , Eid et al. (2017)
      • Eid M.A.
      • Aly S.M.
      • Huneif M.A.
      • Ismail D.K.
      Effect of isokinetic training on muscle strength and postural balance in children with Down’s syndrome.
      , Wijesekara (2013)
      • Wijesekara D.S.
      Clinical approach to a floppy infant.
      , Bay (2006)

      Bay M. Cerebral hypotonia [Internet]. San Diego: Roos RP, chief editor. MedLink Neurology. 12 Jul 2006 [update 2016 Feb 01, cited 2019 Jan 31]. Available from: www.medlink.com.

      , Fahey (2015)
      • Fahey M.
      Floppy baby.
      , Igarashi (2004)
      • Igarashi M.
      Floppy infant syndrome.
      , Ghaffar et al. (2017)
      • Ghaffar H.A.
      • Elawady H.
      • Abouleinin I.
      • Rabie E.
      Diagnostic approach of floppy infants: a study in Fayoum University Hospital, Egypt. Middle East.
      Astasia. Inability to stand due to muscular incoordinationPeredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      Wide-based gaitPeredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      Lack of posture regulationHartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      , Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , Kaur et al. (2016)
      • Kaur J.
      • Punia S.
      Floppy Infant Syndrome: Overview.
      Hip dysplasiaDe Santos-Moreno et al. (2017)
      • De Santos-Moreno M.G.
      • Macias-Merlo M.L.
      • Gómez-Torrón A.
      Programas de bipedestación para la prevención de la displasia de cadera en niños con síndrome de Down [Standing programs for the prevention of hip dysplasia in children with Down syndrome].
      , Jain et al. (2011)
      • Jain R.K.
      • Jayawant S.
      Evaluation of the floppy infant.
      , Sender et al. (2003)
      • Sender P.
      • Jayawant S.
      Evaluation of the floppy infant.
      Frog-like postureHartley et al. (2015)
      • Hartley L.
      • Ranjan R.
      Evaluation of the floppy infant.
      , Peredo et al. (2009)
      • Peredo D.E.
      • Hannibal M.C.
      The floppy infant: evaluation of hypotonia.
      , Naidoo (2013)
      • Naidoo P.
      Current practices in the assesment of hypotonia in children.
      , Reus et al. (2013)
      • Reus L.
      • van Vlimmeren L.A.
      • Staal J.B.
      • et al.
      Objective evaluation of muscle strength in infants with hypotonia and muscle weakness.