Pulmonary outcome measures in long-term survivors of infantile Pompe disease on enzyme replacement therapy: A case series
Mai K. ElMallah
Division of Pulmonary Medicine, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorAnkit K. Desai
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorErica B. Nading
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorStephanie DeArmey
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorRichard M. Kravitz
Division of Pulmonary Medicine, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorCorresponding Author
Priya S. Kishnani
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Correspondence Priya S. Kishnani, Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, NC 27710.
Email: [email protected]
Search for more papers by this authorMai K. ElMallah
Division of Pulmonary Medicine, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorAnkit K. Desai
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorErica B. Nading
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorStephanie DeArmey
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorRichard M. Kravitz
Division of Pulmonary Medicine, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Search for more papers by this authorCorresponding Author
Priya S. Kishnani
Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Correspondence Priya S. Kishnani, Division of Medical Genetics, Department of Pediatrics, Duke University School of Medicine, Durham, NC 27710.
Email: [email protected]
Search for more papers by this authorAbstract
Objectives
To report the respiratory function of school-aged children with infantile Pompe disease (IPD) who started enzyme replacement therapy (ERT) in infancy and early childhood.
Study Design
This is a retrospective chart review of pulmonary function tests of: (a) patients with IPD 5 to 18 years of age, (b) who were not ventilator dependent, and (c) were able to perform upright and supine spirometry. Subjects were divided into a younger (5-9 years) and older cohort (10-18 years) for the analysis. Upright and supine forced vital capacity (FVC), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP) were analyzed.
Results
Fourteen patients, all cross-reactive immunologic material (CRIM)-positive, met the inclusion criteria and were included in this study. Mean upright and supine FVC were 70.3% and 64.9% predicted, respectively, in the 5- to 9-year-old cohort; and 61.5% and 52.5% predicted, respectively, in the 10- to 18-year-old group. Individual patient trends showed stability in FVC overtime in six of the 14 patients. MIPs and MEPs were consistent with inspiratory and expiratory muscle weakness in the younger and older age group but did not decline with age.
Conclusion
Data from this cohort of CRIM-positive patients with IPD showed that ERT is able to maintain respiratory function in a subgroup of patients whereas others had a steady decline. There was a statistically significant decline in FVC from the upright to a supine position in both the younger and older age groups of CRIM-positive ERT-treated patients. Before ERT, patients with IPD were unable to maintain independent ventilation beyond the first few years of life.
CONFLICTS OF INTEREST
PSK has received grant support from Sanofi Genzyme, Valerion Therapeutics, Shire Pharmaceuticals, and Amicus Therapeutics. PSK has received consulting fees and honoraria from Sanofi Genzyme, Shire Pharmaceuticals, Amicus Therapeutics, Vertex Pharmaceuticals, and Asklepios BioPharmaceutical, Inc (AskBio). PSK is a member of the Pompe and Gaucher Disease Registry Advisory Board for Sanofi Genzyme. PSK has equity in Actus Therapeutics, which is developing gene therapy for Pompe disease.
REFERENCES
- 1Hirschhorn R, Reuser AJJ. Glycogen storage disease type II: acid a-glucosidase (acid maltase) deficiency. In: D Valle, CR Scriver, eds. Scriver's OMMBID the online metabolic & molecular bases of inherited disease. New York, NY: McGraw-Hill; 2009.
- 2Kishnani PS, Hwu WL, Mandel H, Nicolino M, Yong F, Corzo D. Infantile-onset Pompe disease natural history study G. A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J Pediatr. 2006; 148: 671-676.
- 3Fuller DD, ElMallah MK, Smith BK, et al. The respiratory neuromuscular system in Pompe disease. Respir Physiol Neurobiol. 2013; 189: 241-249.
- 4van den Hout HM, Hop W, van Diggelen OP, et al. The natural course of infantile Pompe's disease: 20 original cases compared with 133 cases from the literature. Pediatrics. 2003; 112: 332-340.
- 5Slonim AE, Bulone L, Ritz S, Goldberg T, Chen A, Martiniuk F. Identification of two subtypes of infantile acid maltase deficiency. J Pediatr. 2000; 137: 283-285.
- 6 ACMG Work Group on Management of Pompe Disease. Pompe disease diagnosis and management guideline. Genet Med. 2006; 8: 267-288.
- 7Laforet P, Laloui K, Granger B, et al. French Pompe Registry Study G. The French Pompe registry. Baseline characteristics of a cohort of 126 patients with adult Pompe disease. Rev Neurol (Paris). 2013; 169: 595-602.
- 8de Vries JM, van der Beek NA, Hop WC, et al. Effect of enzyme therapy and prognostic factors in 69 adults with Pompe disease: an open-label single-center study. Orphanet J Rare Dis. 2012; 7: 73.
- 9Johnson EM, Roberts M, Mozaffar T, Young P, Quartel A, Berger KI. Pulmonary function tests (maximum inspiratory pressure, maximum expiratory pressure, vital capacity, forced vital capacity) predict ventilator use in late-onset Pompe disease. Neuromuscul Disord. 2016; 26: 136-145.
- 10Berger KI, Chan Y, Rom WN, Oppenheimer BW, Goldring RM. Progression from respiratory dysfunction to failure in late-onset Pompe disease. Neuromuscul Disord. 2016; 26: 481-489.
- 11Alonso-Perez J, Segovia S, Dominguez-Gonzalez C, et al. Spanish Pompe registry: baseline characteristics of first 49 patients with adult onset of Pompe disease. Med Clin. 2019:pii: S0025-7753(19)30346-X.
- 12Hobson-Webb LD, Jones HN, Kishnani PS. Oropharyngeal dysphagia may occur in late-onset Pompe disease, implicating bulbar muscle involvement. Neuromuscul Disord. 2013; 23: 319-323.
- 13Dubrovsky A, Corderi J, Lin M, Kishnani PS, Jones HN. Expanding the phenotype of late-onset Pompe disease: Tongue weakness: A new clinical observation. Muscle Nerve. 2011; 44: 897-901.
- 14Kishnani PS, Corzo D, Nicolino M, et al. Recombinant human acid [alpha]-glucosidase: major clinical benefits in infantile-onset Pompe disease. Neurology. 2007; 68: 99-109.
- 15Kishnani PS, Nicolino M, Voit T, et al. Chinese hamster ovary cell-derived recombinant human acid alpha-glucosidase in infantile-onset Pompe disease. J Pediatr. 2006; 149: 89-97.
- 16Nicolino M, Byrne B, Wraith JE, et al. Clinical outcomes after long-term treatment with alglucosidase alfa in infants and children with advanced Pompe disease. Genet Med. 2009; 11: 210-219.
- 17Kishnani PS, Corzo D, Leslie ND, et al. Early treatment with alglucosidase alpha prolongs long-term survival of infants with Pompe disease. Pediatr Res. 2009; 66: 329-335.
- 18Banugaria SG, Prater SN, Ng YK, et al. The impact of antibodies on clinical outcomes in diseases treated with therapeutic protein: lessons learned from infantile Pompe disease. Genet Med. 2011; 13: 729-736.
- 19Kishnani PS, Goldenberg PC, DeArmey SL, et al. Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol Genet Metab. 2010; 99: 26-33.
- 20Prater SN, Banugaria SG, DeArmey SM, et al. The emerging phenotype of long-term survivors with infantile Pompe disease. Genet Med. 2012; 14: 800-810.
- 21Regnery C, Kornblum C, Hanisch F, et al. 36 months observational clinical study of 38 adult Pompe disease patients under alglucosidase alfa enzyme replacement therapy. J Inherit Metab Dis. 2012; 35: 837-845.
- 22De Filippi P, Saeidi K, Ravaglia S, et al. Genotype-phenotype correlation in Pompe disease, a step forward. Orphanet J Rare Dis. 2014; 9: 102.
- 23Yanovitch TL, Banugaria SG, Proia AD, Kishnani PS. Clinical and histologic ocular findings in Pompe disease. J Pediatr Ophthalmol Strabismus. 2010; 47: 34-40.
- 24Berrier KL, Kazi ZB, Prater SN, et al. CRIM-negative infantile Pompe disease: characterization of immune responses in patients treated with ERT monotherapy. Genet Med. 2015; 17: 912-918.
- 25DeRuisseau LR, Fuller DD, Qiu K, et al. Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc Natl Acad Sci U S A. 2009; 106: 9419-9424.
- 26Byrne BJ, Fuller DD, Smith BK, et al. Pompe disease gene therapy: neural manifestations require consideration of CNS directed therapy. Ann Transl Med. 2019; 7: 290.
- 27Kishnani PS, Hwu WL, Mandel H, et al. A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J Pediatr. 2006; 148: 671-676.
- 28Eigen H, Bieler H, Grant D, et al. Spirometric pulmonary function in healthy preschool children. Am J Respir Crit Care Med. 2001; 163: 619-623.
- 29Miller MR, Hankinson J, Brusasco V, et al. Standardisation of spirometry. Eur Respir J. 2005; 26: 319-338.
- 30Lechtzin N, Wiener CM, Shade DM, Clawson L, Diette GB. Spirometry in the supine position improves the detection of diaphragmatic weakness in patients with amyotrophic lateral sclerosis. Chest. 2002; 121: 436-442.
- 31Baydur A. Respiratory muscle strength: a reliable index for predicting survival in amyotrophic lateral sclerosis? Am J Respir Crit Care Med. 2017; 195: 12-13.
- 32Aldrich TK, Spiro P. Maximal inspiratory pressure: does reproducibility indicate full effort? Thorax. 1995; 50: 40-43.
- 33Hull J, Aniapravan R, Chan E, et al. British Thoracic Society guideline for respiratory management of children with neuromuscular weakness. Thorax. 2012; 67(Suppl 1): i1-i40.
- 34 American Thoracic Society/European Respiratory Society. ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002; 166: 518-624.
- 35Elmallah MK, Falk DJ, Nayak S, et al. Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in Pompe mice. Mol Ther. 2014; 22: 702-712.
- 36Keeler AM, Liu D, Zieger M, et al. Airway smooth muscle dysfunction in Pompe (Gaa-/-) mice. Am J Physiol Lung Cell Mol Physiol. 2017; 312: L873-L881.
- 37ElMallah MK, Pagliardini S, Turner SM, et al. Ampakines stimulate respiratory motor output and ventilation in a murine model of Pompe disease. Am J Respir Cell Mol Biol. 2015; 53: 326-335.
- 38Kuperus E, van der Meijden JC, In 't Groen SLM, et al. The ACE I/D polymorphism does not explain heterogeneity of natural course and response to enzyme replacement therapy in Pompe disease. PLoS One. 2018; 13:e0208854.
- 39Kishnani PS, Beckemeyer AA, Mendelsohn NJ. The new era of Pompe disease: advances in the detection, understanding of the phenotypic spectrum, pathophysiology, and management. Am J Med Genet, Part C. 2012; 160C: 1-7.
- 40Yanovitch TL, Casey R, Banugaria SG, Kishnani PS. Improvement of bilateral ptosis on higher dose enzyme replacement therapy in Pompe disease. J Neuroophthalmol. 2010; 30: 165-166.
- 41van Gelder CM, Poelman E, Plug I, et al. Effects of a higher dose of alglucosidase alfa on ventilator-free survival and motor outcome in classic infantile Pompe disease: an open-label single-center study. J Inherit Metab Dis. 2016; 39: 383-390.
- 42Shea L, Raben N. Autophagy in skeletal muscle: implications for Pompe disease. Int J Clin Pharmacol Ther. 2009; 47(Suppl 1): S42-S47.
- 43Fuller DD, ElMallah MK, Smith BK, Corti M, Falk DJ, Byrne BJ Pompe disease and the respiratory system respiratory physiology and neurobiology 2013; In press.
- 44Sidman RL, Taksir T, Fidler J, et al. Temporal neuropathologic and behavioral phenotype of 6neo/6neo Pompe disease mice. J Neuropathol Exp Neurol. 2008; 67: 803-818.
- 45Lim JA, Yi H, Gao F, Raben N, Kishnani PS, Sun B. Intravenous injection of an AAV-PHP.B vector encoding human acid alpha-glucosidase rescues both muscle and CNS defects in murine Pompe disease. Mol Ther Methods Clin Dev. 2019; 12: 233-245.
- 46Matsui T, Kuroda S, Mizutani M, Kiuchi Y, Suzuki K, Ono T. Generalized glycogen storage disease in Japanese quail (Coturnix coturnix japonica). Vet Pathol. 1983; 20: 312-321.
- 47Qiu K, Falk DJ, Reier PJ, Byrne BJ, Fuller DD. Spinal delivery of AAV vector restores enzyme activity and increases ventilation in Pompe mice. Mol Ther. 2012; 20: 21-27.
- 48Hogan GR, Gutmann L, Schmidt R, Gilbert E. Pompe's disease. Neurology. 1969; 19: 894-900.
- 49Teng YT, Su WJ, Hou JW, Huang SF. Infantile-onset glycogen storage disease type II (Pompe disease): report of a case with genetic diagnosis and pathological findings. Chang Gung Med J. 2004; 27: 379-384.
- 50Mancall EL, Aponte GE, Berry RG. Pompe's disease (diffuse glycogenosis) with neuronal storage. J Neuropathol Exp Neurol. 1965; 24: 85-96.
- 51Thurberg BL, Lynch Maloney C, Vaccaro C, et al. Characterization of pre- and post-treatment pathology after enzyme replacement therapy for Pompe disease. Lab Invest. 2006; 86: 1208-1220.
- 52Pellegrini N, Laforet P, Orlikowski D, et al. Respiratory insufficiency and limb muscle weakness in adults with Pompe's disease. Eur Respir J. 2005; 26: 1024-1031.
- 53David W, Stockton MB, Byrne Barry, et al. Impact of time from diagnosis to treatment on lung function among patients with late-onset Pompe disease: data from the Pompe Registry. Mol Genet Metab. 2019; 126(2): S140. https://doi.org/10.1016/j.ymgme.2018.12.360
- 54Kazi ZB, Desai AK, Berrier KL, et al. Sustained immune tolerance induction in enzyme replacement therapy-treated CRIM-negative patients with infantile Pompe disease. JCI Insight. 2017; 2(16):pii: 94328. https://doi.org/10.1172/jci.insight.94328
- 55Keeler AM, Zieger M, Todeasa S, et al. Systemic delivery of AAVB1-GAA clears glycogen and prolongs survival in a mouse model of Pompe disease. Hum Gene Ther. 2018; 30: 57-68.
- 56Han SO, Ronzitti G, Arnson B, et al. Low-dose liver-targeted gene therapy for Pompe disease enhances therapeutic efficacy of ERT via immune tolerance induction. Mol Ther Methods Clin Dev. 2017; 4: 126-136.
Citing Literature
