{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T16:05:07Z","timestamp":1781712307251,"version":"3.54.5"},"reference-count":28,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2025,8,19]],"date-time":"2025-08-19T00:00:00Z","timestamp":1755561600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,8,19]],"date-time":"2025-08-19T00:00:00Z","timestamp":1755561600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000780","name":"European Union","doi-asserted-by":"crossref","award":["PNRR-MR1-2022-12376937_CUP C53C22001200007"],"award-info":[{"award-number":["PNRR-MR1-2022-12376937_CUP C53C22001200007"]}],"id":[{"id":"10.13039\/501100000780","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000780","name":"European Union","doi-asserted-by":"crossref","award":["PNRR-MR1-2022-12376937_CUP C53C22001200007"],"award-info":[{"award-number":["PNRR-MR1-2022-12376937_CUP C53C22001200007"]}],"id":[{"id":"10.13039\/501100000780","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000780","name":"European Union","doi-asserted-by":"crossref","award":["PNRR-MR1-2022-12376937_CUP C53C22001200007"],"award-info":[{"award-number":["PNRR-MR1-2022-12376937_CUP C53C22001200007"]}],"id":[{"id":"10.13039\/501100000780","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100005743","name":"Universit\u00e0 Cattolica del Sacro Cuore","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100005743","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Eur J Pediatr"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The advent of newborn screening for spinal muscular atrophy (SMA) has highlighted the need for easy, quick, clinical tools to be used in infants with SMA identified in the neonatal period. We propose a new short module developed using items from the Hammersmith Neonatal Neurological Examination (HNNE) and from a module developed for floppy infants, both previously used in newborns with SMA. The new module was developed by identifying and selecting the items that were more often found to have abnormal findings in SMA newborns. The proforma was designed by selecting 13 items and converting them into a format that would facilitate the interpretation of the results. The cohort included 25 infants. Based on HNNE and add-on module results, 13 were classified as asymptomatic, 5 as pauci-symptomatic, and 7 as symptomatic. All symptomatic infants showed abnormalities in posture, tone, tremors, and reflexes, along with reduced antigravity movements and abnormal breathing. Among pauci-symptomatic infants, all had abnormal reflexes, three also had tremors, and one showed mild hypotonia. There was excellent inter-observer reliability assessed using intra-class correlation coefficients with 95% confidence intervals (0.947) and full concordance with the original full-length forms.<\/jats:p>\n                  <jats:p>\n                    <jats:italic>Conclusion<\/jats:italic>\n                    : Our findings support the use of the short form in clinical practice, especially when time or resources are limited. It can be used in multiple occasions, allowing to detect the onset of possible signs in asymptomatic infants and to follow their progression.\n                    <jats:table-wrap>\n                      <jats:table>\n                        <jats:tbody>\n                          <jats:tr>\n                            <jats:td colspan=\"2\">\n                              <jats:bold>What is Known:<\/jats:bold>\n                              <jats:italic>\u2022 Newborns with SMA identified by neonatal screening may show clinical signs at diagnosis.<\/jats:italic>\n                              <jats:italic>\u2022 These signs may be subtle and easily missed on standard neonatal examination.<\/jats:italic>\n                              <jats:bold>What is New:<\/jats:bold>\n                              <jats:italic>\u2022 The new form includes a short examination that can reliably detect initial signs of SMA.<\/jats:italic>\n                              <jats:italic>\u2022 The new examination can be used to detect the onset and the progression of clinical signs.<\/jats:italic>\n                            <\/jats:td>\n                          <\/jats:tr>\n                        <\/jats:tbody>\n                      <\/jats:table>\n                    <\/jats:table-wrap>\n                  <\/jats:p>","DOI":"10.1007\/s00431-025-06382-4","type":"journal-article","created":{"date-parts":[[2025,8,18]],"date-time":"2025-08-18T23:47:42Z","timestamp":1755560862000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Development of\u00a0the \u201cSMA NNE,\u201d a short\u00a0neonatal neurological examination for newborns\u00a0with spinal muscular atrophy"],"prefix":"10.1007","volume":"184","author":[{"given":"Eugenio","family":"Mercuri","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giorgia","family":"Coratti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Costanza","family":"Cutrona","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberto","family":"De Sanctis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giulia","family":"Stanca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gianpaolo","family":"Cicala","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marianna","family":"Villa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Capasso","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Arpaia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina","family":"Sbarbati","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristin","family":"Krosschell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Domenico","family":"Romeo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Beatrice","family":"Berti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard","family":"Finkel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marika","family":"Pane","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,8,19]]},"reference":[{"key":"6382_CR1","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1038\/s41572-022-00380-8","volume":"8","author":"E Mercuri","year":"2022","unstructured":"Mercuri E, Sumner CJ, Muntoni F, Darras BT, Finkel RS (2022) Spinal muscular atrophy. Nat Rev Dis Primers 8:52","journal-title":"Nat Rev Dis Primers"},{"key":"6382_CR2","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1002\/ana.25101","volume":"82","author":"SJ Kolb","year":"2017","unstructured":"Kolb SJ, Coffey CS, Yankey JW, Krosschell K, Arnold WD, Rutkove SB, Swoboda KJ et al (2017) Natural history of infantile-onset spinal muscular atrophy. Ann Neurol 82:883\u2013891","journal-title":"Ann Neurol"},{"key":"6382_CR3","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1212\/WNL.0000000000000741","volume":"83","author":"RS Finkel","year":"2014","unstructured":"Finkel RS, McDermott MP, Kaufmann P, Darras BT, Chung WK, Sproule DM, Kang PB, Foley AR, Yang ML, Martens WB, Oskoui M, Glanzman AM, Flickinger J, Montes J, Dunaway S, O\u2019Hagen J, Quigley J, Riley S, Benton M, Ryan PA, Montgomery M, Marra J, Gooch C, De Vivo DC (2014) Observational study of spinal muscular atrophy type I and implications for clinical trials. Neurology 83:810\u2013817","journal-title":"Neurology"},{"key":"6382_CR4","doi-asserted-by":"publisher","first-page":"2247","DOI":"10.1093\/brain\/awac125","volume":"145","author":"RS Finkel","year":"2022","unstructured":"Finkel RS, Benatar M (2022) Pre-symptomatic spinal muscular atrophy: a proposed nosology. Brain 145:2247\u20132249","journal-title":"Brain"},{"key":"6382_CR5","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/0960-8966(91)90051-S","volume":"1","author":"V Dubowitz","year":"1991","unstructured":"Dubowitz V (1991) Chaos in classification of the spinal muscular atrophies of childhood. Neuromuscul Disord 1:77\u201380","journal-title":"Neuromuscul Disord"},{"key":"6382_CR6","volume-title":"Muscle disorders in childhood","author":"V Dubowitz","year":"1995","unstructured":"Dubowitz V (1995) Muscle disorders in childhood, 2nd edn. WB Saunders, London","edition":"2"},{"key":"6382_CR7","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/S1090-3798(99)80012-9","volume":"3","author":"V Dubowitz","year":"1999","unstructured":"Dubowitz V (1999) Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur J Paediatr Neurol 3:49\u201351","journal-title":"Eur J Paediatr Neurol"},{"key":"6382_CR8","doi-asserted-by":"publisher","first-page":"2821","DOI":"10.1007\/s00431-022-04470-3","volume":"181","author":"M Pane","year":"2022","unstructured":"Pane M, Donati MA, Cutrona C, De Sanctis R, Pirinu M, Coratti G, Ricci M, Palermo C, Berti B, Leone D, Ticci C, Sacchini M, Cerboneschi M, Capasso A, Cicala G, Pera MC, Bravetti C, Abiusi E, Vaisfeld A, Vento G, Tiziano FD, Mercuri E (2022) Neurological assessment of newborns with spinal muscular atrophy identified through neonatal screening. Eur J Pediatr 181:2821\u20132829","journal-title":"Eur J Pediatr"},{"key":"6382_CR9","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1016\/j.nmd.2019.09.007","volume":"29","author":"DC De Vivo","year":"2019","unstructured":"De Vivo DC, Bertini E, Swoboda KJ, Hwu WL, Crawford TO, Finkel RS, Kirschner J et al (2019) Nusinersen initiated in infants during the presymptomatic stage of spinal muscular atrophy: interim efficacy and safety results from the phase 2 NURTURE study. Neuromuscul Disord 29:842\u2013856","journal-title":"Neuromuscul Disord"},{"key":"6382_CR10","doi-asserted-by":"publisher","first-page":"19922","DOI":"10.1038\/s41598-021-99496-2","volume":"11","author":"F Boemer","year":"2021","unstructured":"Boemer F, Caberg JH, Beckers P, Dideberg V, di Fiore S, Bours V, Marie S, Dewulf J, Marcelis L, Deconinck N, Daron A, Blasco-Perez L, Tizzano E, Hiligsmann M, Lombet J, Pereira T, Lopez-Granados L, Shalchian-Tehran S, van Assche V, Willems A, Huybrechts S, Mast B, van Olden R, Dangouloff T, Servais L (2021) Three years pilot of spinal muscular atrophy newborn screening turned into official program in Southern Belgium. Sci Rep 11:19922","journal-title":"Sci Rep"},{"key":"6382_CR11","doi-asserted-by":"publisher","first-page":"574","DOI":"10.1016\/j.nmd.2021.03.007","volume":"31","author":"T Dangouloff","year":"2021","unstructured":"Dangouloff T, Vrscaj E, Servais L, Osredkar D, Group SNWS (2021) Newborn screening programs for spinal muscular atrophy worldwide: where we stand and where to go. Neuromuscul Disord 31:574\u2013582","journal-title":"Neuromuscul Disord"},{"key":"6382_CR12","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1016\/S0022-3476(98)70279-3","volume":"133","author":"L Dubowitz","year":"1998","unstructured":"Dubowitz L, Mercuri E, Dubowitz V (1998) An optimality score for the neurologic examination of the term newborn. J Pediatr 133:406\u2013416","journal-title":"J Pediatr"},{"key":"6382_CR13","doi-asserted-by":"publisher","first-page":"2771","DOI":"10.1007\/s00431-022-04476-x","volume":"181","author":"C Cutrona","year":"2022","unstructured":"Cutrona C, Pede E, De Sanctis R, Coratti G, Tiberi E, Luciano R, Pera MC, Velli C, Capasso A, Vento G, Romeo DM, Pane M, Mercuri E (2022) Assessing floppy infants: a new module. Eur J Pediatr 181:2771\u20132778","journal-title":"Eur J Pediatr"},{"key":"6382_CR14","doi-asserted-by":"publisher","first-page":"2995","DOI":"10.1007\/s00431-024-05546-y","volume":"183","author":"M Pane","year":"2024","unstructured":"Pane M, Stanca G, Ticci C, Cutrona C, De Sanctis R, Pirinu M, Coratti G et al (2024) Early neurological signs in infants identified through neonatal screening for SMA: do they predict outcome? Eur J Pediatr 183:2995\u20132999","journal-title":"Eur J Pediatr"},{"key":"6382_CR15","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.1016\/j.jpeds.2012.07.037","volume":"161","author":"DM Romeo","year":"2012","unstructured":"Romeo DM, Ricci D, van Haastert IC, de Vries LS, Haataja L, Brogna C, Gallini F, Romagnoli C, Cowan FM, Mercuri E (2012) Neurologic assessment tool for screening preterm infants at term age. J Pediatr 161:1166\u20131168","journal-title":"J Pediatr"},{"key":"6382_CR16","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1179\/027249302125002029","volume":"22","author":"L Haataja","year":"2002","unstructured":"Haataja L, McGready R, Arunjerdja R, Simpson JA, Mercuri E, Nosten F, Dubowitz L (2002) A new approach for neurological evaluation of infants in resource-poor settings. Ann Trop Paediatr 22:355\u2013368","journal-title":"Ann Trop Paediatr"},{"key":"6382_CR17","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1067\/mpd.2003.215","volume":"142","author":"E Mercuri","year":"2003","unstructured":"Mercuri E, Guzzetta A, Laroche S, Ricci D, vanhaastert I, Simpson A, Luciano R, Bleakley C, Frisone MF, Haataja L, Tortorolo G, Guzzetta F, de Vries L, Cowan F, Dubowitz L (2003) Neurologic examination of preterm infants at term age: comparison with term infants. J Pediatr 142:647\u2013655","journal-title":"J Pediatr"},{"key":"6382_CR18","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1055\/s-2007-1004520","volume":"38","author":"DM Romeo","year":"2007","unstructured":"Romeo DM, Cioni M, Guzzetta A, Scoto M, Conversano M, Palermo F, Romeo MG, Mercuri E (2007) Application of a scorable neurological examination to near-term infants: longitudinal data. Neuropediatrics 38:233\u2013238","journal-title":"Neuropediatrics"},{"key":"6382_CR19","doi-asserted-by":"crossref","unstructured":"Dubowitz LM, Cowan F, Rutherford M, Mercuri E, Pennock J (1995) Neonatal neurology, past present and future. A window on the brain. Brain Dev 17(Suppl):22\u201330","DOI":"10.1016\/0387-7604(95)90067-5"},{"key":"6382_CR20","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.jpeds.2004.08.047","volume":"146","author":"I Vasta","year":"2005","unstructured":"Vasta I, Kinali M, Messina S, Guzzetta A, Kapellou O, Manzur A, Cowan F, Muntoni F, Mercuri E (2005) Can clinical signs identify newborns with neuromuscular disorders? J Pediatr 146:73\u201379","journal-title":"J Pediatr"},{"issue":"124\u2013129","key":"6382_CR21","first-page":"e121","volume":"190","author":"YH Chien","year":"2017","unstructured":"Chien YH, Chiang SC, Weng WC, Lee NC, Lin CJ, Hsieh WS, Lee WT, Jong YJ, Ko TM, Hwu WL (2017) Presymptomatic diagnosis of spinal muscular atrophy through newborn screening. J Pediatr 190(124\u2013129):e121","journal-title":"J Pediatr"},{"key":"6382_CR22","doi-asserted-by":"publisher","first-page":"1070","DOI":"10.1016\/j.nmd.2021.07.008","volume":"31","author":"T Dangouloff","year":"2021","unstructured":"Dangouloff T, Boemer F, Servais L (2021) Newborn screening of neuromuscular diseases. Neuromuscul Disord 31:1070\u20131080","journal-title":"Neuromuscul Disord"},{"key":"6382_CR23","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1038\/s41436-019-0673-0","volume":"22","author":"DST Kariyawasam","year":"2020","unstructured":"Kariyawasam DST, Russell JS, Wiley V, Alexander IE, Farrar MA (2020) The implementation of newborn screening for spinal muscular atrophy: the Australian experience. Genet Med 22:557\u2013565","journal-title":"Genet Med"},{"key":"6382_CR24","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1038\/gim.2017.152","volume":"20","author":"JN Kraszewski","year":"2018","unstructured":"Kraszewski JN, Kay DM, Stevens CF, Koval C, Haser B, Ortiz V, Albertorio A, Cohen LL, Jain R, Andrew SP, Young SD, LaMarca NM, De Vivo DC, Caggana M, Chung WK (2018) Pilot study of population-based newborn screening for spinal muscular atrophy in New York state. Genet Med 20:608\u2013613","journal-title":"Genet Med"},{"key":"6382_CR25","doi-asserted-by":"publisher","first-page":"932","DOI":"10.1002\/acn3.779","volume":"6","author":"BT Darras","year":"2019","unstructured":"Darras BT, Crawford TO, Finkel RS, Mercuri E, De Vivo DC, Oskoui M, Tizzano EF, Ryan MM, Muntoni F, Zhao G, Staropoli J, McCampbell A, Petrillo M, Stebbins C, Fradette S, Farwell W, Sumner CJ (2019) Neurofilament as a potential biomarker for spinal muscular atrophy. Ann Clin Transl Neurol 6:932\u2013944","journal-title":"Ann Clin Transl Neurol"},{"key":"6382_CR26","doi-asserted-by":"publisher","first-page":"85","DOI":"10.3233\/JND-221644","volume":"11","author":"C Cutrona","year":"2024","unstructured":"Cutrona C, de Sanctis R, Coratti G, Capasso A, Ricci M, Stanca G, Carnicella S, Utlulig M, Bersani G, Lazzareschi I, Leoni C, Buonsenso D, Luciano R, Vento G, Finkel RS, Pane M, Mercuri E (2024) Can the CHOP-INTEND be used as an outcome measure in the first months of age? Implications for clinical trials and real world data. J Neuromuscul Dis 11:85\u201390","journal-title":"J Neuromuscul Dis"},{"key":"6382_CR27","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1111\/dmcn.14798","volume":"63","author":"R Masson","year":"2021","unstructured":"Masson R, Brusa C, Scoto M, Baranello G (2021) Brain, cognition, and language development in spinal muscular atrophy type 1: a scoping review. Dev Med Child Neurol 63:527\u2013536","journal-title":"Dev Med Child Neurol"},{"key":"6382_CR28","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1136\/archdischild-2023-326613","volume":"109","author":"B Buchignani","year":"2024","unstructured":"Buchignani B, Cicala G, Cumbo F, Ricci M, Capasso A, Ticci C, Mazzanti S, Brolatti N, Tosi M, Dosi C, Antonaci L, Coratti G, Pera MC, Leone D, Palermo C, Berti B, Frongia AL, Sacchini M, Bruno C, Masson R, D\u2019Amico A, Battini R, Pane M, Mercuri E (2024) Communicative development inventory in type 1 and presymptomatic infants with spinal muscular atrophy: a cohort study. Arch Dis Child 109:395\u2013401","journal-title":"Arch Dis Child"}],"container-title":["European Journal of Pediatrics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00431-025-06382-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00431-025-06382-4","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00431-025-06382-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,27]],"date-time":"2026-03-27T15:09:56Z","timestamp":1774624196000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00431-025-06382-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,19]]},"references-count":28,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2025,9]]}},"alternative-id":["6382"],"URL":"https:\/\/doi.org\/10.1007\/s00431-025-06382-4","relation":{},"ISSN":["1432-1076"],"issn-type":[{"value":"1432-1076","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,19]]},"assertion":[{"value":"16 July 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 July 2025","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 August 2025","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 August 2025","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of the Catholic University of Rome (prot. N. 003,475\/21).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Written informed consent was obtained in all cases.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}}],"article-number":"562"}}