Newborn Screening for Krabbe Disease and Other Lysosomal Storage Disorders: Broad Lessons Learned
Abstract
:1. Introduction
2. Background
3. Therapies
4. Newborn Screening
4.1. Krabbe Disease
4.2. Pompe Disease
4.3. Missouri LSD Screening
5. Krabbe Disease Screening in NY—Analytical Challenges
5.1. Analytical Challenges in LSD Screening
5.2. Second-Tier Molecular Testing
5.3. Screening for LSDs with Late Onset Forms
5.4. Referred Infants and the Challenges of Diagnostic Testing
5.5. Psychosine Testing
5.6. Diagnostic Evaluations
6. Summary
Acknowledgments
Conflicts of Interest
References
- Orsini, J.J.; Kay, D.M.; Saavedra-Matiz, C.A.; Duffner, P.K.; Erbe, R.W.; Biski, C.; Martin, M.; Krein, L.M.; Nichols, M.; Kurtzberg, J.; et al. New York State Krabbe Disease Consortium. Newborn screening for Krabbe disease in New York State: The first eight years’ experience. Genet. Med. 2016, 18, 239–248. [Google Scholar] [CrossRef] [PubMed]
- Wasserstein, M.P.; Andriola, M.; Arnold, G.; Aron, A.; Duffner, P.; Erbe, R.W.; Escolar, M.L.; Estrella, L.; Galvin-Parton, P.; Iglesias, A.; et al. New York State Krabbe Consortium. 2016. Outcomes of Children with Abnormal Newborn Screens for Krabbe Disease. Genet. Med. 2016. [Google Scholar] [CrossRef]
- Orsini, J.J.; Saavedra-Matiz, C.A.; Gelb, M.H.; Caggana, M. Newborn Screening for Krabbe Disease. J. Neurosci. Res. 2016. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Brockman, K.; Turecek, F.; Scott, C.R.; Gelb, M.H. Tandem mass spectrometry for the direct assay of enzymes in dried blood spots: Application to newborn screening for Krabbe Disease. Clin. Chem. 2004, 50, 638–640. [Google Scholar] [CrossRef] [PubMed]
- Wenger, D.; Escolar, M.L.; Luzi, P.; Rafi, M.A. Krabbe Disease (Globoid Cell Leukodystrophy). In The Online Metabolic and Molecular Bases of Inherited Diseases; Valle, D.B.A., Vogelstein, B., Kinzler, K.W., Antonarakis, S.E., Ballabio, A., Eds.; McGraw-Hill: New York, NY, USA, 2013. [Google Scholar]
- Escolar, M.L.; Poe, M.D.; Provenzale, J.M.; Richards, K.C.; Allison, J.; Wood, S.; Wenger, D.A.; Pietryga, D.; Wall, D.; Champagne, M.; et al. Transplantation of umbilical-cord blood in babies with infantile Krabbe’s disease. N. Engl. J. Med. 2005, 352, 2069–2081. [Google Scholar] [CrossRef] [PubMed]
- Wang, R.Y.; Bodamer, O.A.; Watson, M.S.; Wilcox, W.R.; ACMG Work Group on Diagnostic Confirmation of Lysosomal Storage Diseases. Lysosomal storage diseases: Diagnostic confirmation and management of presymptomatic individuals. Genet. Med. 2011, 13, 457–484. [Google Scholar] [CrossRef] [PubMed]
- Marsden, D.; Levy, H. Newborn Screening for lysosomal storage disorders. Clin. Chem. 2010, 56, 1071–1079. [Google Scholar] [CrossRef] [PubMed]
- Parenti, G.; Pignata, C.; Vajro, P.; Salerno, M. New strategies for the treatment of lysosomal storage diseases. Int. J. Mol. Med. 2013, 1, 11–20. [Google Scholar] [CrossRef] [PubMed]
- Brady, R.O.; Pentchev, P.G.; Gal, A.E.; Hibbert, S.R.; Dekaban, A.S. Replacment therapy for inherited enzyme deficiency. Use of purified glucocerebrosidase in Gaucher’s disease. N. Engl. J. Med. 1974, 291, 989–993. [Google Scholar] [CrossRef] [PubMed]
- Desnick, R.J.; Schuchman, E.H. Enzyme replacement therapy for lysosomal diseases: Lessons from 20 years of experience and remaining challenges. Annu. Rev. Genom. Hum. Genet. 2012, 13, 307–335. [Google Scholar] [CrossRef] [PubMed]
- Hobbs, J.R.; Hugh-Jones, K.; Barrett, A.J.; Byrom, N.; Chambers, D.; Henry, K.; James, D.C.; Lucas, C.F.; Rogers, T.R.; Benson, P.F.; et al. Reversal of clinical features of Hurler’s disease and biochemical improvement after treatment by bone-marrow transplantation. Lancet 1981, 2, 709–712. [Google Scholar] [CrossRef]
- Cox, T.M. Inovative treatments for lysosomal diseases. Best Pract. Res. Clin. Endocrinol. Metab. 2015, 2, 275–311. [Google Scholar] [CrossRef] [PubMed]
- Macauley, S.L. Combination Therapies for Lysosomal Storage Diseases: A Complex Answer to a Simple Problem. Pediatr. Endocrinol. Rev. 2016, 1, 639–648. [Google Scholar]
- Rastall, D.P.; Amalfitano, A. Recent advances in gene therapy for lysosomal storage disorders. Appl. Clin. Genet. 2015, 24, 157–169. [Google Scholar]
- Coutinho, M.F.; Santos, J.I.; Alves, S. Less is More: Substrate Reduction Therapy for Lysosomal Storage Disorders. J. Mol. Sci. 2016, 17, 1–22. [Google Scholar] [CrossRef] [PubMed]
- Ranierri, E.; Gerace, R.L.; Ravenscroft, E.M.; Hopwood, J.J.; Meikle, P.J. Pilot neonatal screening program for lysosomal storage disorders, using lamp-1. Southeast Asian J. Trop. Med. Public Health 1999, 30 (Suppl. S2), 111–113. [Google Scholar] [PubMed]
- Hua, C.T.; Hopwood, J.J.; Carlsson, S.R.; Harris, R.J.; Meikle, P.J. Evaluation of the lysosome-associated membrane protein LAMP-2 as a marker for lysosomal storage disorders. Clin. Chem. 1998, 10, 2094–2102. [Google Scholar]
- Chamoles, N.A.; Blanco, M.; Gaggioli, D. Diagnosis of α-l-iduronidase deficiency in dried blood spots on filter paper: The possibility of newborn diagnosis. Clin. Chem. 2001, 47, 780–781. [Google Scholar] [PubMed]
- Chamoles, N.A.; Blanco, M.B.; Gaggioli, D.; Casentini, C. Hurler-like phenotype: Enzymatic diagnosis in dried blood spots on filter paper. Clin. Chem. 2001, 12, 2098–2102. [Google Scholar]
- Chamoles, N.A.; Niizawa, G.; Blanco, M.; Gaggioli, D.; Casentini, C. Glycogen storage disease type II: Enzymatic screening in dried blood spots on filter paper. Clin. Chim. Acta 2004, 347, 97–102. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Scott, C.R.; Chamoles, N.A.; Ghavami, A.; Pinto, B.M.; Turecek, F.; Gelb, M.H. Direct multiplex assay of lysosomal enzymes in dried blood spots for newborn screening. Clin. Chem. 2004, 50, 1785–1796. [Google Scholar] [CrossRef] [PubMed]
- Chien, Y.H.; Chiang, S.C.; Zhang, X.K.; Keutzer, J.; Lee, N.C.; Huang, A.C.; Chen, C.A.; Wu, M.H.; Huang, P.H.; Tsai, F.J.; et al. Early detection of Pompe disease by newborn screening is feasible: Results from the Taiwan screening program. Pediatrics 2008, 122, 39–45. [Google Scholar] [CrossRef] [PubMed]
- Liao, H.C.; Chiang, C.C.; Niu, D.M.; Wang, C.H.; Kao, S.M.; Tsai, F.J.; Huang, Y.H.; Liu, H.C.; Huang, C.K.; Gao, H.J.; et al. Detecting multiple lysosomal storage diseases by tandem mass spectrometry—A national newborn screening program in Taiwan. Clin. Chim. Acta 2014, 431, 80–86. [Google Scholar] [CrossRef] [PubMed]
- Chien, Y.H.; Lee, N.C.; Huang, H.J.; Thurberg, B.L.; Tsai, F.J.; Hwu, W.L. Later-onset Pompe disease: Early detection and early treatment initiation enabled by newborn screening. J. Pediatr. 2011, 158, 1023–1027. [Google Scholar] [CrossRef] [PubMed]
- Hopkins, P.V.; Campbell, C.; Klug, T.; Rogers, S.; Raburn-Miller, J.; Kiesling, J. Lysosomal storage disorder screening implementation: Findings from the first six months of full population pilot testing in Missouri. J. Pediatr. 2015, 166, 172–177. [Google Scholar] [CrossRef] [PubMed]
- Spada, M.; Pagliardini, S.; Yasuda, M.; Tukel, T.; Thiagarajan, G.; Sakuraba, H.; Ponzone, A.; Desnick, R.J. High incidence of later-onset Fabry disease revealed by newborn screening. Am. J. Hum. Genet. 2006, 79, 31–40. [Google Scholar] [CrossRef] [PubMed]
- Lin, H.Y.; Chong, K.W.; Hsu, J.H.; Yu, H.C.; Shih, C.C.; Huang, C.H.; Lin, S.J.; Chen, C.H.; Chiang, C.C.; Ho, H.J.; et al. High incidence of the cardiac variant of Fabry disease revealed by newborn screening in the Taiwan Chinese population. Circ. Cardiovasc. Genet. 2009. [Google Scholar] [CrossRef] [PubMed]
- Wittmann, J.; Karg, E.; Turi, S.; Legnini, E.; Wittmann, G.; Giese, A.K.; Lukas, J.; Gölnitz, U.; Klingenhäger, M.; Bodamer, O.; et al. Newborn screening for lysosomal storage disorders in Hungary. JIMD Rep. 2012, 6, 117–125. [Google Scholar] [PubMed]
- Mechtler, T.P.; Stary, S.; Metz, T.F.; De Jesús, V.R.; Greber-Platzer, S.; Pollak, A.; Herkner, K.R.; Streubel, B.; Kasper, D.C. Neonatal screening for lysosomal storage disorders: Feasibility and incidence from a nationwide study in Austria. Lancet 2012, 379, 335–341. [Google Scholar] [CrossRef]
- Elliott, S.; Buroker, N.; Cournoyer, J.J.; Potier, A.M.; Trometer, J.D.; Elbin, C.; Schermer, M.J.; Kantola, J.; Boyce, A.; Turecek, F.; et al. Pilot study of newborn screening for six lysosomal storage diseases using Tandem Mass Spectrometry. Mol. Genet. Metab. 2016, 118, 304–309. [Google Scholar] [CrossRef] [PubMed]
- Eble, B.E.; et al. Harriet Lane Handbook, 15th ed.; Tschudy, M.M., Arcara, K.M., Eds.; Mosby, Inc.: St Louis, MO, USA, 2000; pp. 325–326. [Google Scholar]
- Orsini, J.J.; Yeman, J.; Caggana, M.; Bodamer, O.A.; Mühl, A. Semi-quantitative method for determination of hematocrit in dried blood spots, using data collected in HPLC hemoglobin variant testing. Clin. Chim. Acta 2010, 411, 894–895. [Google Scholar] [CrossRef] [PubMed]
- Duffey, T.A.; Bellamy, G.; Elliott, S.; Fox, A.C.; Glass, M.; Turecek, F.; Gelb, M.H.; Scott, C.R. A tandem mass spectrometry triplex assay for the detection of Fabry, Pompe, and mucopolysaccharidosis-I (Hurler). Clin. Chem. 2010, 56, 1854–1861. [Google Scholar] [CrossRef] [PubMed]
- Mørkrid, L.; Rowe, A.D.; Elgstoen, K.B.P.; Olesen, J.H.; Ruijter, G.; Hall, P.L.; Tortorelli, S.; Schulze, A.; Kyriakopoulou, L.; Wamelink, M.M.; et al. Continuous age- and gender-adjusted reference intervals of urinary markers for cerebral creatine deficiency syndromes: A novel approach to the definition of reference intervals. Clin. Chem. 2015, 61, 760–768. [Google Scholar] [CrossRef] [PubMed]
- Marquardt, G.; Currier, R.; McHugh, D.M.S.; Gavrilov, D.; Magera, M.J.; Matern, D.; Oglesbee, D.; Raymond, K.; Rinaldo, P.; Smith, E.H.; et al. Enhanced interpretation of newborn screening results without analyte cutoff values. Genet. Med. 2012, 14, 648–654. [Google Scholar] [CrossRef] [PubMed]
- Hall, P.L.; Marquardt, G.; McHugh, D.M.; Currier, R.J.; Tang, H.; Stoway, S.D.; Rinaldo, P. Post-analytical tools improve performance of newborn screening by tandem mass spectrometry. Genet. Med. 2014, 16, 889–895. [Google Scholar] [CrossRef] [PubMed]
- Wenger, D.A.; Luzi, P.; Rafi, M.A. Krabbe disease: Are certain mutations disease-causing only when specific polymorphisms are present or when inherited in trans with specific second mutations? Mol. Genet. Metab. 2014, 111, 307–308. [Google Scholar] [CrossRef] [PubMed]
- Musumeci, O.; Thieme, A.; Claeys, K.G.; Wenninger, S.; Kley, R.A.; Kuhn, M.; Lukacs, Z.; Deschauer, M.; Gaeta, M.; Toscano, A.; et al. Homozygosity for the common GAA gene splice site mutation c.-32–13T>G in Pompe disease is associated with the classical adult phenotypical spectrum. Neuromuscul. Disord. 2015, 25, 719–724. [Google Scholar] [CrossRef] [PubMed]
- Cooper, D.N.; Krawczak, M.; Polychronakos, C.; Tyler-Smith, C.; Kehrer-Sawatzk, H. Where genotype is not predictive of phenotype: Towards an understanding of the molecular basis of reduced penetrance in human inherited disease. Hum. Genet. 2013, 132, 1077–1130. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; Sakai, N.; Taniike, M.; Inui, K.; Ozono, K. Six novel mutations detected in the GALC gene in 17 Japanese patients with Krabbe disease, and new genotype-phenotype correlation. J. Hum. Genet. 2006, 51, 548–554. [Google Scholar] [CrossRef] [PubMed]
- Saavedra-Matiz, C.A.; Luzi, P.; Nichols, M.; Orsini, J.J.; Caggana, M.; Wenger, D.A. Expression of individual mutations and haplotypes in the galactocerebrosidase gene identified by the newborn screening program in New York State and in confirmed cases of Krabbe’s disease. J. Neurosci. Res. 2016, 94, 1076–1083. [Google Scholar] [CrossRef] [PubMed]
- Weinreich, S.S.; Rigter, T.; van El, C.G.; Dondorp, W.J.; Kostense, P.J.; van der Ploeg, A.T.; Reuser, A.J.; Cornel, M.C.; Hagemans, M.L. Public support for neonatal screening for Pompe disease, a broad-phenotype condition. Orphanet J. Rare Dis. 2012, 14, 7–15. [Google Scholar] [CrossRef] [PubMed]
- Chuang, W.L.; Pacheco, J.; Zhang, X.K.; Martin, M.M.; Biski, C.K.; Keutzer, J.M.; Wenger, D.A.; Caggana, M.; Orsini, J.J. Determination of psychosine concentration in dried blood spots from newborns that were identified via newborn screening to be at risk for Krabbe disease. Clin. Chim. Acta 2013, 419, 73–76. [Google Scholar] [CrossRef] [PubMed]
- Turgeon, C.T.; Orsini, J.J.; Sanders, K.A.; Magera, M.J.; Langan, T.J.; Escolar, M.L.; Duffner, P.; Oglesbee, D.; Gavrilov, D.; Tortorelli, S.; et al. Measurement of psychosine in dried blood spots—A possible improvement to newborn screening programs for Krabbe disease. J. Inherit. Metab. Dis. 2015, 38, 923–929. [Google Scholar] [CrossRef] [PubMed]
- Carter, R.L.; Wrabetz, L.; Jalal, K.; Orsini, J.J.; Barczykowski, A.L.; Matern, D.; Langan, T.J. Can psychosine and galactocerebrosidase activity predict early-infantile Krabbe′s disease presymptomatically? J. Neurosci. Res. 2016, 94, 1084–1093. [Google Scholar] [CrossRef] [PubMed]
- Johnson, B.; Mascher, H.; Mascher, D.; Legnini, E.; Hung, C.Y.; Dajnoki, A.; Chien, Y.H.; Maródi, L.; Hwu, W.L.; Bodamer, O.A. Analysis of lyso-globotriaosylsphingosine in dried blood spots. Ann. Lab. Med. 2013, 33, 274–278. [Google Scholar] [CrossRef] [PubMed]
- Raymond, K.M.; Turgeon, C.; Ory, D.; Lourenco, C.; Giugliani, R.; Rinaldo, P.; Gavrilov, D.; Oglesbee, D.; Tortorelli, S.; Matern, D. Combined analysis of plasma oxysterol and lysosphingomyelin for Niemann–Pick types A, B and C diagnosis. J. Inherit. Metab. Dis. 2015, 38, S36. [Google Scholar]
- de Ruijter, J.; de Ru, M.H.; Wagemans, T.; Ijlst, L.; Lund, A.M.; Orchard, P.J.; Schaefer, G.B.; Wijburg, F.A.; van Vlies, N. Heparan sulfate and dermatan sulfate derived disaccharides are sensitive markers for newborn screening for mucopolysaccharidoses types I, II and III. Mol. Genet. Metab. 2012, 107, 705–710. [Google Scholar] [CrossRef] [PubMed]
- Weinstock, N.I.; Wrabetz, L.; Feltri, M.L.; Shin, D. Metabolic profiling reveals biochemical pathways and potential biomarkers associated with the pathogenesis of Krabbe disease. J. Neurosci. Res. 2016, 94, 1094–1107. [Google Scholar] [CrossRef] [PubMed]
<20% Initial Analyte | Average 6-Plex %DMA | Avg of Extra Enzymes | |||||
---|---|---|---|---|---|---|---|
GALC | IDUA | GLA | ABG | ASM | GAA | ||
GALC | 18.0 | 64.1 | 57.8 | 58.3 | 86.0 | 69.0 | 67.0 |
GAA | 61.7 | 47.0 | 69.2 | 50.7 | 67.8 | 17.5 | 59.3 |
Population Average | 100 | 100 | 100 | 100 | 100 | 100 |
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Orsini, J.J.; Caggana, M. Newborn Screening for Krabbe Disease and Other Lysosomal Storage Disorders: Broad Lessons Learned. Int. J. Neonatal Screen. 2017, 3, 3. https://doi.org/10.3390/ijns3010003
Orsini JJ, Caggana M. Newborn Screening for Krabbe Disease and Other Lysosomal Storage Disorders: Broad Lessons Learned. International Journal of Neonatal Screening. 2017; 3(1):3. https://doi.org/10.3390/ijns3010003
Chicago/Turabian StyleOrsini, Joseph J., and Michele Caggana. 2017. "Newborn Screening for Krabbe Disease and Other Lysosomal Storage Disorders: Broad Lessons Learned" International Journal of Neonatal Screening 3, no. 1: 3. https://doi.org/10.3390/ijns3010003