Prevalence, incidence and carrier frequency of 5q-linked spinal muscular atrophy - A literature review

Orphanet Journal of Rare Diseases

Volumn 12, Issue 1, 2017, Pages

  Verhaart, Ingrid E C ^a   Robertson, Agata ^a   Wilson, Ian J ^a   Aartsma Rus, Annemieke ^a   Cameron, Shona ^a   Jones, Cynthia C ^b   Cook, Suzanne F ^c   Lochmüller, Hanns ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b BIOGEN   (United States)

^c Epidemiology Assoc LLC   (United States)

Author keywords

Carrier frequency; Ethnic background; Incidence; Prevalence; Spinal muscular atrophy

Indexed keywords

ASIAN; BLACK PERSON; CAUCASIAN; CHROMOSOME 5Q; COPY NUMBER VARIATION; DIAGNOSTIC ACCURACY; DISEASE SEVERITY; GENE; GENE MUTATION; GENETIC SCREENING; HETEROZYGOTE; HUMAN; MORBIDITY; PHENOTYPE; PREVALENCE; REVIEW; SMN1 GENE; SPINAL MUSCULAR ATROPHY; CHROMOSOME 5; ETHNOLOGY; FEMALE; GENETICS; INCIDENCE; MALE;

SMN1 PROTEIN, HUMAN; SURVIVAL MOTOR NEURON PROTEIN 1;

CHROMOSOMES, HUMAN, PAIR 5; FEMALE; HUMANS; INCIDENCE; MALE; MUSCULAR ATROPHY, SPINAL; PREVALENCE; SURVIVAL OF MOTOR NEURON 1 PROTEIN;

EID: 85021659386     PISSN: None     EISSN: 17501172     Source Type: Journal    
DOI: 10.1186/s13023-017-0671-8     Document Type: Review

References (116)

1. Finkel R, Bertini E, Muntoni F, Mercuri E. 209th ENMC international workshop: outcome measures and clinical trial readiness in spinal muscular atrophy 7-9 November 2014, Heemskerk, The Netherlands. Neuromuscul Disord. 2015;25:593-602.
2. Mercuri E, Bertini E, Iannaccone ST. Childhood spinal muscular atrophy: controversies and challenges. Lancet Neurol. 2012;11:443-52.
3. Lefebvre S, Burglen L, Reboullet S, Clermont O, Burlet P, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80:155-65.
4. Wirth B, Herz M, Wetter A, Moskau S, Hahnen E, et al. Quantitative analysis of survival motor neuron copies: identification of subtle SMN1 mutations in patients with spinal muscular atrophy, genotype-phenotype correlation, and implications for genetic counseling. Am J Hum Genet. 1999;64:1340-56.
5. Alias L, Bernal S, Fuentes-Prior P, Barcelo MJ, Also E, et al. Mutation update of spinal muscular atrophy in Spain: molecular characterization of 745 unrelated patients and identification of four novel mutations in the SMN1 gene. Hum Genet. 2009;125:29-39.
6. Burglen L, Lefebvre S, Clermont O, Burlet P, Viollet L, et al. Structure and organization of the human survival motor neurone (SMN) gene. Genomics. 1996;32:479-82.
7. Wirth B, Garbes L, Riessland M. How genetic modifiers influence the phenotype of spinal muscular atrophy and suggest future therapeutic approaches. Curr Opin Genet Dev. 2013;23:330-8.
8. Feldkotter M, Schwarzer V, Wirth R, Wienker TF, Wirth B. Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet. 2002;70:358-68.
9. Wirth B, Brichta L, Schrank B, Lochmuller H, Blick S, et al. Mildly affected patients with spinal muscular atrophy are partially protected by an increased SMN2 copy number. Hum Genet. 2006;119:422-8.
10. Ahn EJ, Yum MS, Kim EH, Yoo HW, Lee BH, et al. Genotype-phenotype correlation of SMN1 and NAIP deletions in Korean patients with spinal muscular atrophy. J Clin Neurol. 2016
11. Amara A, Adala L, Ben Charfeddine I, Mamai O, Mili A, et al. Correlation of SMN2, NAIP, p44, H4F5 and Occludin genes copy number with spinal muscular atrophy phenotype in Tunisian patients. Eur J Paediatr Neurol. 2012;16:167-74.
12. He J, Zhang QJ, Lin QF, Chen YF, Lin XZ, et al. Molecular analysis of SMN1, SMN2, NAIP, GTF2H2, and H4F5 genes in 157 Chinese patients with spinal muscular atrophy. Gene. 2013;518:325-9.
13. Oprea GE, Krober S, McWhorter ML, Rossoll W, Muller S, et al. Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science. 2008;320:524-7.
14. Scharf JM, Endrizzi MG, Wetter A, Huang S, Thompson TG, et al. Identification of a candidate modifying gene for spinal muscular atrophy by comparative genomics. Nat Genet. 1998;20:83-6.
15. Watihayati MS, Fatemeh H, Marini M, Atif AB, Zahiruddin WM, et al. Combination of SMN2 copy number and NAIP deletion predicts disease severity in spinal muscular atrophy. Brain Dev. 2009;31:42-5.
16. Roy N, Mahadevan MS, McLean M, Shutler G, Yaraghi Z, et al. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell. 1995;80:167-78.
17. Hosseinibarkooie S, Peters M, Torres-Benito L, Rastetter RH, Hupperich K, et al. The power of human protective modifiers: PLS3 and CORO1C unravel impaired Endocytosis in spinal muscular atrophy and rescue SMA phenotype. Am J Hum Genet. 2016;99:647-65.
18. FDA approves first drug for spinal muscular atrophy [ http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm534611.htm ].
19. SPINRAZA® (Nusinersen) Approved in the European Union as First Treatment for Spinal Muscular Atrophy [ http://media.biogen.com/press-release/investor-relations/spinraza-nusinersen-approved-european-union-first-treatment-spinal- ].
20. Lunn MR, Wang CH. Spinal muscular atrophy. Lancet. 2008;371:2120-33.
21. Ogino S, Leonard DG, Rennert H, Ewens WJ, Wilson RB. Genetic risk assessment in carrier testing for spinal muscular atrophy. Am J Med Genet. 2002;110:301-7.
22. Merlini L, Stagni SB, Marri E, Granata C. Epidemiology of neuromuscular disorders in the under-20 population in Bologna Province, Italy. Neuromuscul Disord. 1992;2:197-200.
23. Arkblad E, Tulinius M, Kroksmark AK, Henricsson M, Darin N. A population-based study of genotypic and phenotypic variability in children with spinal muscular atrophy. Acta Paediatr. 2009;98:865-72.
24. Darin N, Tulinius M. Neuromuscular disorders in childhood: a descriptive epidemiological study from western Sweden. Neuromuscul Disord. 2000;10:1-9.
25. Tangsrud SE, Halvorsen S. Child neuromuscular disease in southern Norway. Prevalence, age and distribution of diagnosis with special reference to «non-Duchenne muscular dystrophy». Clin Genet. 1988;34:145-52.
26. Ahlstrom G, Gunnarsson LG, Leissner P, Sjoden PO. Epidemiology of neuromuscular diseases, including the postpolio sequelae, in a Swedish county. Neuroepidemiology. 1993;12:262-9.
27. Hagberg B, Westerberg B. Hereditary motor and sensory neuropathies in Swedish children. I. Prevalence and distribution by disability groups. Acta Paediatr Scand. 1983;72:379-83.
28. Wesstrom G, Bensch J, Schollin J. Congenital myotonic dystrophy. Incidence, clinical aspects and early prognosis. Acta Paediatr Scand. 1986;75:849-54.
29. al Rajeh S, Bademosi O, Ismail H, Awada A, Dawodu A, et al. A community survey of neurological disorders in Saudi Arabia: the Thugbah study. Neuroepidemiology. 1993;12:164-78.
30. Ogino S, Wilson RB, Gold B. New insights on the evolution of the SMN1 and SMN2 region: simulation and meta-analysis for allele and haplotype frequency calculations. Eur J Hum Genet. 2004;12:1015-23.
31. Chung B, Wong V, Ip P. Prevalence of neuromuscular diseases in Chinese children: a study in southern China. J Child Neurol. 2003;18:217-9.
32. Norwood FL, Harling C, Chinnery PF, Eagle M, Bushby K, Straub V. Prevalence of genetic muscle disease in Northern England: in-depth analysis of a muscle clinic population. Brain. 2009;132:3175-86.
33. Thieme A, Mitulla B, Schulze F, Spiegler AW. Epidemiological data on Werdnig-Hoffmann disease in Germany (West-Thuringen). Hum Genet. 1993;91:295-7.
34. Vaidla E, Talvik I, Kulla A, Kahre T, Hamarik M, et al. Descriptive epidemiology of spinal muscular atrophy type I in Estonia. Neuroepidemiology. 2006;27:164-8.
35. Finkel RS, McDermott MP, Kaufmann P, Darras BT, Chung WK, et al. Observational study of spinal muscular atrophy type I and implications for clinical trials. Neurology. 2014;83:810-7.
36. Oskoui M, Levy G, Garland CJ, Gray JM, O'Hagen J, et al. The changing natural history of spinal muscular atrophy type 1. Neurology. 2007;69:1931-6.
37. Chung BH, Wong VC, Ip P. Spinal muscular atrophy: survival pattern and functional status. Pediatrics. 2004;114:e548-53.
38. Zerres K, Rudnik-Schoneborn S. Natural history in proximal spinal muscular atrophy. Clinical analysis of 445 patients and suggestions for a modification of existing classifications. Arch Neurol. 1995;52:518-23.
39. Zerres K, Rudnik-Schoneborn S, Forrest E, Lusakowska A, Borkowska J, Hausmanowa-Petrusewicz I. A collaborative study on the natural history of childhood and juvenile onset proximal spinal muscular atrophy (type II and III SMA): 569 patients. J Neurol Sci. 1997;146:67-72.
40. Farrar MA, Park SB, Vucic S, Carey KA, Turner BJ, et al. Emerging therapies and challenges in spinal muscular atrophy. Ann Neurol. 2017;81:355-68.
41. Pearn J. Incidence, prevalence, and gene frequency studies of chronic childhood spinal muscular atrophy. J Med Genet. 1978;15:409-13.
42. Spiegler AW, Hausmanowa-Pertrusewicz I, Borkowska J, Klopocka A. Population data on acute infantile and chronic childhood spinal muscular atrophy in Warsaw. Hum Genet. 1990;85:211-4.
43. Thieme A, Mitulla B, Schulze F, Spiegler AW. Chronic childhood spinal muscular atrophy in Germany (West-Thuringen) - an epidemiological study. Hum Genet. 1994;93:344-6.
44. Kvasnicova M, Stykova J, Hudec P. Incidence of spinal muscular atrophy and Duchenne's muscular dystrophy in the juvenile population of central Slovakia. Bratisl Lek Listy. 1994;95:78-82.
45. Zaldivar T, Montejo Y, Acevedo AM, Guerra R, Vargas J, et al. Evidence of reduced frequency of spinal muscular atrophy type I in the Cuban population. Neurology. 2005;65:636-8.
46. Hendrickson BC, Donohoe C, Akmaev VR, Sugarman EA, Labrousse P, et al. Differences in SMN1 allele frequencies among ethnic groups within North America. J Med Genet. 2009;46:641-4.
47. MacDonald WK, Hamilton D, Kuhle S. SMA carrier testing: a meta-analysis of differences in test performance by ethnic group. Prenat Diagn. 2014;34:1219-26.
48. Radhakrishnan K, Thacker AK, Maloo JC. A clinical, epidemiological and genetic study of hereditary motor neuropathies in Benghazi, Libya. J Neurol. 1988;235:422-4.
49. Emery AE. Population frequencies of inherited neuromuscular diseases - a world survey. Neuromuscul Disord. 1991;1:19-29.
50. Czeizel A, Hamula J. A hungarian study on Werdnig-Hoffmann disease. J Med Genet. 1989;26:761-3.
51. Ignatius J, Donner M. Epidemiology of childhood disorders (in Finnish). In: H L, editor. Lihastautien Kehittyvä Tutkimus Ja Hoito. Turku: Kiasma; 1989.
52. Pearn JH. The gene frequency of acute Werdnig-Hoffmann disease (SMA type 1). A total population survey in North-East England. J Med Genet. 1973;10:260-5.
53. Burd L, Short SK, Martsolf JT, Nelson RA. Prevalence of type I spinal muscular atrophy in North Dakota. Am J Med Genet. 1991;41:212-5.
54. Kurland LT. Descriptive epidemiology of selected neurologic and myopathic disorders with particular reference to a survey in Rochester, Minnesota. J Chronic Dis. 1958;8:378-418.
55. Zellweger H, Hanhart E. The infantile proximal spinal muscular atrophies in Switzerland. Helv Paediatr Acta. 1972;27:355-60.
56. Ogino S, Wilson RB. Spinal muscular atrophy: molecular genetics and diagnostics. Expert Rev Mol Diagn. 2004;4:15-29.
57. Prior TW, Nagan N, Sugarman EA, Batish SD, Braastad C. Technical standards and guidelines for spinal muscular atrophy testing. Genet Med. 2011;13:686-94.
58. Butchbach ME. Copy number variations in the survival motor neuron genes: implications for spinal muscular atrophy and other neurodegenerative diseases. Front Mol Biosci. 2016;3:7.
59. Kuzma-Kozakiewicz M, Jedrzejowska M, Kazmierczak B. SMN1 gene duplications are more frequent in patients with progressive muscular atrophy. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:457-62.
60. Ben-Shachar S, Orr-Urtreger A, Bardugo E, Shomrat R, Yaron Y. Large-scale population screening for spinal muscular atrophy: clinical implications. Genet Med. 2011;13:110-4.
61. Su YN, Hung CC, Lin SY, Chen FY, Chern JP, et al. Carrier screening for spinal muscular atrophy (SMA) in 107,611 pregnant women during the period 2005-2009: a prospective population-based cohort study. PLoS One. 2011;6:e17067.
62. Sugarman EA, Nagan N, Zhu H, Akmaev VR, Zhou Z, et al. Pan-ethnic carrier screening and prenatal diagnosis for spinal muscular atrophy: clinical laboratory analysis of >72,400 specimens. Eur J Hum Genet. 2012;20:27-32.
63. Sukenik-Halevy R, Pesso R, Garbian N, Magal N, Shohat M. Large-scale population carrier screening for spinal muscular atrophy in Israel - effect of ethnicity on the false-negative rate. Genet Test Mol Biomarkers. 2010;14:319-24.
64. Zlotogora J, Grotto I, Kaliner E, Gamzu R. The Israeli national population program of genetic carrier screening for reproductive purposes. Genet Med. 2016;18:203-6.
65. Labrum R, Rodda J, Krause A. The molecular basis of spinal muscular atrophy (SMA) in South African black patients. Neuromuscul Disord. 2007;17:684-92.
66. Sangare M, Hendrickson B, Sango HA, Chen K, Nofziger J, et al. Genetics of low spinal muscular atrophy carrier frequency in sub-Saharan Africa. Ann Neurol. 2014;75:525-32.
67. Sheng-Yuan Z, Xiong F, Chen YJ, Yan TZ, Zeng J, et al. Molecular characterization of SMN copy number derived from carrier screening and from core families with SMA in a Chinese population. Eur J Hum Genet. 2010;18:978-84.
68. Chan V, Yip B, Yam I, Au P, Lin CK, et al. Carrier incidence for spinal muscular atrophy in southern Chinese. J Neurol. 2004;251:1089-93.
69. Contreras-Capetillo SN, Blanco HL, Cerda-Flores RM, Lugo-Trampe J, Torres-Munoz I, et al. Frequency of deletion carriers in a Mestizo population of central and northeastern Mexico: a pilot study. Exp Ther Med. 2015;9:2053-8.
70. Goncalves-Rocha M, Oliveira J, Rodrigues L, Santos R. New approaches in molecular diagnosis and population carrier screening for spinal muscular atrophy. Genet Test Mol Biomarkers. 2011;15:319-26.
71. Landaburu I, Gonzalvo MC, Clavero A, Ramirez JP, Yoldi A, et al. Genetic testing of sperm donors for cystic fibrosis and spinal muscular atrophy: evaluation of clinical utility. Eur J Obstet Gynecol Reprod Biol. 2013;170:183-7.
72. Cali F, Ruggeri G, Chiavetta V, Scuderi C, Bianca S, et al. Carrier screening for spinal muscular atrophy in Italian population. J Genet. 2014;93:179-81.
73. Jedrzejowska M, Milewski M, Zimowski J, Zagozdzon P, Kostera-Pruszczyk A, et al. Incidence of spinal muscular atrophy in Poland - more frequent than predicted? Neuroepidemiology. 2010;34:152-7.
74. Lyahyai J, Sbiti A, Barkat A, Ratbi I, Sefiani A. Spinal muscular atrophy carrier frequency and estimated prevalence of the disease in Moroccan newborns. Genet Test Mol Biomarkers. 2012;16:215-8.
75. Wang KC, Chang CC, Chang YF, Wang SH, Chiang CK, Tsai CP. Evaluation and characterization of a high-resolution melting analysis kit for rapid carrier-screening test of spinal muscular atrophy. J Neurogenet. 2015;29:113-6.
76. Chen TH, Tzeng CC, Wang CC, Wu SM, Chang JG, et al. Identification of bidirectional gene conversion between SMN1 and SMN2 by simultaneous analysis of SMN dosage and hybrid genes in a Chinese population. J Neurol Sci. 2011;308:83-7.
77. Luo M, Liu L, Peter I, Zhu J, Scott SA, et al. An Ashkenazi Jewish SMN1 haplotype specific to duplication alleles improves pan-ethnic carrier screening for spinal muscular atrophy. Genet Med. 2014;16:149-56.
78. Callum P, Iger J, Ray M, Sims CA, Falk RE. Outcome and experience of implementing spinal muscular atrophy carrier screening on sperm donors. Fertil Steril. 2010;94:1912-4.
79. Bueno KC, Gouvea SP, Genari AB, Funayama CA, Zanette DL, et al. Detection of spinal muscular atrophy carriers in a sample of the Brazilian population. Neuroepidemiology. 2011;36:105-8.
80. Larson JL, Silver AJ, Chan D, Borroto C, Spurrier B, Silver LM. Validation of a high resolution NGS method for detecting spinal muscular atrophy carriers among phase 3 participants in the 1000 genomes project. BMC Med Genet. 2015;16:100.
81. Chong JX, Oktay AA, Dai Z, Swoboda KJ, Prior TW, Ober C. A common spinal muscular atrophy deletion mutation is present on a single founder haplotype in the US Hutterites. Eur J Hum Genet. 2011;19:1045-51.
82. Anhuf D, Eggermann T, Rudnik-Schoneborn S, Zerres K. Determination of SMN1 and SMN2 copy number using TaqMan technology. Hum Mutat. 2003;22:74-8.
83. Corcia P, Camu W, Halimi JM, Vourc'h P, Antar C, et al. SMN1 gene, but not SMN2, is a risk factor for sporadic ALS. Neurology. 2006;67:1147-50.
84. Corcia P, Ingre C, Blasco H, Press R, Praline J, et al. Homozygous SMN2 deletion is a protective factor in the Swedish ALS population. Eur J Hum Genet. 2012;20:588-91.
85. Cusin V, Clermont O, Gerard B, Chantereau D, Elion J. Prevalence of SMN1 deletion and duplication in carrier and normal populations: implication for genetic counselling. J Med Genet. 2003;40:e39.
86. Gerard B, Ginet N, Matthijs G, Evrard P, Baumann C, et al. Genotype determination at the survival motor neuron locus in a normal population and SMA carriers using competitive PCR and primer extension. Hum Mutat. 2000;16:253-63.
87. Veldink JH, Kalmijn S, Van der Hout AH, Lemmink HH, Groeneveld GJ, et al. SMN genotypes producing less SMN protein increase susceptibility to and severity of sporadic ALS. Neurology. 2005;65:820-5.
88. Veldink JH, van den Berg LH, Cobben JM, Stulp RP, De Jong JM, et al. Homozygous deletion of the survival motor neuron 2 gene is a prognostic factor in sporadic ALS. Neurology. 2001;56:749-52.
89. Basel-Vanagaite L, Taub E, Drasinover V, Magal N, Brudner A, et al. Genetic carrier screening for spinal muscular atrophy and spinal muscular atrophy with respiratory distress 1 in an isolated population in Israel. Genet Test. 2008;12:53-6.
90. Chen KL, Wang YL, Rennert H, Joshi I, Mills JK, et al. Duplications and de novo deletions of the SMNt gene demonstrated by fluorescence-based carrier testing for spinal muscular atrophy. Am J Med Genet. 1999;85:463-9.
91. Hasanzad M, Azad M, Kahrizi K, Saffar BS, Nafisi S, et al. Carrier frequency of SMA by quantitative analysis of the SMN1 deletion in the Iranian population. Eur J Neurol. 2010;17:160-2.
92. Huang CH, Chang YY, Chen CH, Kuo YS, Hwu WL, et al. Copy number analysis of survival motor neuron genes by multiplex ligation-dependent probe amplification. Genet Med. 2007;9:241-8.
93. Lee TM, Kim SW, Lee KS, Jin HS, Koo SK, et al. Quantitative analysis of SMN1 gene and estimation of SMN1 deletion carrier frequency in Korean population based on real-time PCR. J Korean Med Sci. 2004;19:870-3.
94. Mailman MD, Heinz JW, Papp AC, Snyder PJ, Sedra MS, et al. Molecular analysis of spinal muscular atrophy and modification of the phenotype by SMN2. Genet Med. 2002;4:20-6.
95. Majumdar R, Rehana Z, Al Jumah M, Fetaini N. Spinal muscular atrophy carrier screening by multiplex polymerase chain reaction using dried blood spot on filter paper. Ann Hum Genet. 2005;69:216-21.
96. McAndrew PE, Parsons DW, Simard LR, Rochette C, Ray PN, et al. Identification of proximal spinal muscular atrophy carriers and patients by analysis of SMNT and SMNC gene copy number. Am J Hum Genet. 1997;60:1411-22.
97. Yoon S, Lee CH, Lee KA. Determination of SMN1 and SMN2 copy numbers in a Korean population using multiplex ligation-dependent probe amplification. Korean J Lab Med. 2010;30:93-6.
98. Ogino S, Leonard DG, Rennert H, Wilson RB. Spinal muscular atrophy genetic testing experience at an academic medical center. J Mol Diagn. 2002;4:53-8.
99. Smith M, Calabro V, Chong B, Gardiner N, Cowie S, du Sart D. Population screening and cascade testing for carriers of SMA. Eur J Hum Genet. 2007;15:759-66.
100. Wirth B, Schmidt T, Hahnen E, Rudnik-Schoneborn S, Krawczak M, et al. De novo rearrangements found in 2% of index patients with spinal muscular atrophy: mutational mechanisms, parental origin, mutation rate, and implications for genetic counseling. Am J Hum Genet. 1997;61:1102-11.
101. Prior TW, Snyder PJ, Rink BD, Pearl DK, Pyatt RE, et al. Newborn and carrier screening for spinal muscular atrophy. Am J Med Genet A. 2010;152A:1608-16.
102. Jedrzejowska M, Borkowska J, Zimowski J, Kostera-Pruszczyk A, Milewski M, et al. Unaffected patients with a homozygous absence of the SMN1 gene. Eur J Hum Genet. 2008;16:930-4.
103. Prior TW, Swoboda KJ, Scott HD, Hejmanowski AQ. Homozygous SMN1 deletions in unaffected family members and modification of the phenotype by SMN2. Am J Med Genet A. 2004;130A:307-10.
104. Jones C, Cook S, Hobby K, Jarecki J. SMA subtype concordance in siblings: findings from the cure SMA cohort. Neuromuscul Disord. 2016
105. Cobben JM, van der Steege G, Grootscholten P, de Visser M, Scheffer H, Buys CH. Deletions of the survival motor neuron gene in unaffected siblings of patients with spinal muscular atrophy. Am J Hum Genet. 1995;57:805-8.
106. DiDonato CJ, Ingraham SE, Mendell JR, Prior TW, Lenard S, et al. Deletion and conversion in spinal muscular atrophy patients: is there a relationship to severity? Ann Neurol. 1997;41:230-7.
107. Hahnen E, Forkert R, Marke C, Rudnik-Schoneborn S, Schonling J, et al. Molecular analysis of candidate genes on chromosome 5q13 in autosomal recessive spinal muscular atrophy: evidence of homozygous deletions of the SMN gene in unaffected individuals. Hum Mol Genet. 1995;4:1927-33.
108. Somerville MJ, Hunter AG, Aubry HL, Korneluk RG, MacKenzie AE, Surh LC. Clinical application of the molecular diagnosis of spinal muscular atrophy: deletions of neuronal apoptosis inhibitor protein and survival motor neuron genes. Am J Med Genet. 1997;69:159-65.
109. Wang CH, Xu J, Carter TA, Ross BM, Dominski MK, et al. Characterization of survival motor neuron (SMNT) gene deletions in asymptomatic carriers of spinal muscular atrophy. Hum Mol Genet. 1996;5:359-65.
110. Hughes MI, Hicks EM, Nevin NC, Patterson VH. The prevalence of inherited neuromuscular disease in Northern Ireland. Neuromuscul Disord. 1996;6:69-73.
111. Winsor EJ, Murphy EG, Thompson MW, Reed TE. Genetics of childhood spinal muscular atrophy. J Med Genet. 1971;8:143-8.
112. Ludvigsson P, Olafsson E, Hauser WA. Spinal muscular atrophy. Incidence in Iceland. Neuroepidemiology. 1999;18:265-9.
113. MacMillan JC, Harper PS. Single-gene neurological disorders in South Wales: an epidemiological study. Ann Neurol. 1991;30:411-4.
114. Mostacciuolo ML, Danieli GA, Trevisan C, Muller E, Angelini C. Epidemiology of spinal muscular atrophies in a sample of the Italian population. Neuroepidemiology. 1992;11:34-8.
115. Pascalet-Guidon MJ, Bois E, Feingold J, Mattei JF, Combes JC, Hamon C. Cluster of acute infantile spinal muscular atrophy (Werdnig-Hoffmann disease) in a limited area of Reunion Island. Clin Genet. 1984;26:39-42.
116. Fried K, Mundel G. High incidence of spinal muscular atrophy type I (Werdnig - Hoffmann disease) in the Karaite community in Israel. Clin Genet. 1977;12:250-1.