Inspiratory muscle conditioning exercise and diaphragm gene therapy in Pompe disease: Clinical evidence of respiratory plasticity

Experimental Neurology

Volumn 287, Issue , 2017, Pages 216-224

  Smith, Barbara K ^a,b   Martin, A Daniel ^a   Lawson, Lee Ann ^b   Vernot, Valerie ^c   Marcus, Jordan ^a   Islam, Saleem ^b   Shafi, Nadeem ^d   Corti, Manuela ^b   Collins, Shelley W ^b   Byrne, Barry J ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c NONE   (United States)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Diaphragm; Gene therapy; Pompe disease; Ventilatory insufficiency

Indexed keywords

GLUCAN 1,4 ALPHA GLUCOSIDASE; PARVOVIRUS VECTOR; ALPHA GLUCOSIDASE;

ADOLESCENT; ARTICLE; ARTIFICIAL VENTILATION; CHILD; DIAPHRAGM MOVEMENT; DIAPHRAGMATIC GENE THERAPY; ELECTROMYOGRAM; ENZYME REPLACEMENT; EXERCISE; GENE THERAPY; GLYCOGEN STORAGE DISEASE TYPE 2; HUMAN; INSPIRATORY MUSCLE CONDITIONING EXERCISE; INSPIRATORY PRESSURE; INSPIRATORY THRESHOLD LOAD; INSPIRED TIDAL VOLUME; LOAD COMPENSATION; LUNG VENTILATION; MAXIMAL INSPIRATORY PRESSURE; MOTONEURON; NEUROLOGIC DISEASE; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; OUTCOME ASSESSMENT; PEAK INSPIRATORY FLOW; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHRENIC MOTONEURON; PRESCHOOL CHILD; PRIORITY JOURNAL; RESPIRATORY FUNCTION; RESPIRATORY NEURAL DYSFUNCTION; RESPIRATORY TRACT PARAMETERS; SCHOOL CHILD; VIRAL GENE DELIVERY SYSTEM; ADENOVIRIDAE; CLINICAL TRIAL; COMPLICATION; DIAGNOSTIC IMAGING; DIAPHRAGM; ELECTROMYOGRAPHY; FEMALE; GENETICS; GLYCOGEN STORAGE DISEASE TYPE II; KINESIOTHERAPY; MALE; METABOLISM; PATHOPHYSIOLOGY; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PHYSIOLOGY; PROSPECTIVE STUDY; RESPIRATORY INSUFFICIENCY; SKELETAL MUSCLE; TREATMENT OUTCOME;

ADENOVIRIDAE; ADOLESCENT; ALPHA-GLUCOSIDASES; CHILD; CHILD, PRESCHOOL; DIAPHRAGM; ELECTROMYOGRAPHY; EXERCISE THERAPY; FEMALE; GENETIC THERAPY; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MUSCLE, SKELETAL; PROSPECTIVE STUDIES; RESPIRATORY INSUFFICIENCY; TREATMENT OUTCOME;

EID: 84995901378     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2016.07.013     Document Type: Article

References (32)

1. Byrne, P.I., Collins, S., Mah, C.C., Smith, B., Conlon, T., Martin, S.D., Corti, M., Cleaver, B., Islam, S., Lawson, L.A., Phase I/II trial of diaphragm delivery of recombinant adeno-associated virus acid alpha-glucosidase (rAAaV1-CMV-GAA) gene vector in patients with Pompe disease. Human Gene Therapy. Clinical Development 25 (2014), 134–163.
2. Carlucci, A., Ceriana, P., Prinianakis, G., Fanfulla, F., Colombo, R., Nava, S., Determinants of weaning success in patients with prolonged mechanical ventilation. Crit. Care, 13, 2009, R97.
3. de Melo-Martin, I., Sondhi, D., Crystal, R.G., When ethics constrains clinical research: trial design of control arms in “greater than minimal risk:” pediatric trials. Hum. Gene Ther. 22 (2011), 1121–1127.
4. DeRuisseau, L.R., Fuller, D.D., Qiu, K., DeRuisseau, K.C., Donnelly, W.H. Jr., Mah, C., Reier, P.J., Byrne, B.J., Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 9419–9424.
5. Falk, D.J., Mah, C.S., Soustek, M.S., Lee, K.Z., Elmallah, M.K., Cloutier, D.A., Fuller, D.D., Byrne, B.J., Intrapleural administration of AAV9 improves neural and cardiorespiratory function in Pompe disease. Mol. Ther. 21 (2013), 1661–1667.
6. Fukuda, T., Ewan, L., Bauer, M., Mattaliano, R.J., Zaal, K., Ralston, E., Plotz, P.H., Raben, N., Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann. Neurol. 59 (2006), 700–708.
7. Gaeta, M., Musumeci, O., Mondello, S., Ruggeri, P., Montagnese, F., Cucinotta, M., Vinci, S., Milardi, D., Toscano, A., Clinical and pathophysiological clues of respiratory dysfunction in late-onset Pompe disease: new insights from a comparative study by MRI and respiratory function assessment. Neuromuscul. Disord. 25 (2015), 852–858.
8. Geiger, P.C., Cody, M.J., Macken, R.L., Sieck, G.C., Maximum specific force depends on myosin heavy chain content in rat diaphragm muscle fibers. J. Appl. Physiol. 89 (2000), 695–703.
9. Harikumar, G., Moxham, J., Greenough, A., Rafferty, G.F., Measurement of maximal inspiratory pressure in ventilated children. Pediatr. Pulmonol. 43 (2008), 1085–1091.
10. Jones, H.N., Crisp, K.D., Moss, T., Strollo, K., Robey, R., Sank, J., Canfield, M., Case, L.E., Mahler, L., Kravitz, R.M., Kishnani, P.S., Effects of respiratory muscle training (RMT) in children with infantile-onset Pompe disease and respiratory muscle weakness. J. Pediatr. Rehabil. Med. 7 (2014), 255–265.
11. Jones, H.N., Crisp, K.D., Robey, R.R., Case, L.E., Kravitz, R.M., Kishnani, P.S., Respiratory muscle training (RMT) in late-onset Pompe disease (LOPD): Effects of training and detraining. Mol. Genet. Metab. 117:2 (2016), 120–128.
12. Kessler, P.D., Podsakoff, G.M., Chen, X., McQuiston, S.A., Colosi, P.C., Matelis, L.A., Kurtzman, G.J., Byrne, B.J., Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 14082–14087.
13. Kikuchi, T., Yang, H.W., Pennybacker, M., Ichihara, N., Mizutani, M., Van Hove, J.L., Chen, Y.T., Clinical and metabolic correction of pompe disease by enzyme therapy in acid maltase-deficient quail. J. Clin. Invest. 101 (1998), 827–833.
14. Kishnani, P.S., Nicolino, M., Voit, T., Rogers, R.C., Tsai, A.C., Waterson, J., Herman, G.E., Amalfitano, A., Thurberg, B.L., Richards, S., Davison, M., Corzo, D., Chen, Y.T., Chinese hamster ovary cell-derived recombinant human acid alpha-glucosidase in infantile-onset Pompe disease. J. Pediatr. 149 (2006), 89–97.
15. Mah, C.S., Falk, D.J., Germain, S.A., Kelley, J.S., Lewis, M.A., Cloutier, D.A., DeRuisseau, L.R., Conlon, T.J., Cresawn, K.O., Fraites, T.J. Jr., Campbell-Thompson, M., Fuller, D.D., Byrne, B.J., Gel-mediated delivery of AAV1 vectors corrects ventilatory function in Pompe mice with established disease. Mol. Ther. 18 (2010), 502–510.
16. Mantilla, C.B., Seven, Y.B., Zhan, W.Z., Sieck, G.C., Diaphragm motor unit recruitment in rats. Respir. Physiol. Neurobiol. 173 (2010), 101–106.
17. Mulreany, L.T., Weiner, D.J., McDonough, J.M., Panitch, H.B., Allen, J.L., Noninvasive measurement of the tension-time index in children with neuromuscular disease. J. Appl. Physiol. 95 (2003), 931–937.
18. Nicolino, M., Byrne, B., Wraith, J.E., Leslie, N., Mandel, H., Freyer, D.R., Arnold, G.L., Pivnick, E.K., Ottinger, C.J., Robinson, P.H., Loo, J.C., Smitka, M., Jardine, P., Tato, L., Chabrol, B., McCandless, S., Kimura, S., Mehta, L., Bali, D., Skrinar, A., Morgan, C., Rangachari, L., Corzo, D., Kishnani, P.S., Clinical outcomes after long-term treatment with alglucosidase alfa in infants and children with advanced Pompe disease. Genitourin. Med. 11 (2009), 210–219.
19. Peterson, D.K., Nochomovitz, M.L., Stellato, T.A., Mortimer, J.T., Long-term intramuscular electrical activation of the phrenic nerve: safety and reliability. IEEE Trans. Biomed. Eng. 41 (1994), 1115–1126.
20. Prater, S.N., Banugaria, S.G., DeArmey, S.M., Botha, E.G., Stege, E.M., Case, L.E., Jones, H.N., Phornphutkul, C., Wang, R.Y., Young, S.P., Kishnani, P.S., The emerging phenotype of long-term survivors with infantile Pompe disease. Genitourin. Med. 14 (2012), 800–810.
21. Raben, N., Plotz, P., Byrne, B.J., Acid alpha-glucosidase deficiency (glycogenosis type II, Pompe disease). Curr Mol Med 2 (2002), 145–166.
22. Raben, N., Danon, M., Gilbert, A.L., Dwivedi, S., Collins, B., Thurberg, B.L., Mattaliano, R.J., Nagaraju, K., Plotz, P.H., Enzyme replacement therapy in the mouse model of Pompe disease. Mol. Genet. Metab. 80 (2003), 159–169.
23. Sassoon, C.S., What are the implications of blunted load compensation responses in prolonged-weaning patients?. Respir. Care 59 (2014), 129–132.
24. Shea, L., Raben, N., Autophagy in skeletal muscle: implications for Pompe disease. Int. J. Clin. Pharmacol. Ther. 47:Suppl. 1 (2009), S42–S47.
25. Smina, M., Salam, A., Khamiees, M., Gada, P., Amoateng-Adjepong, Y., Manthous, C.A., Cough peak flows and extubation outcomes. Chest 124 (2003), 262–268.
26. Smith, B.K., Collins, S.W., Conlon, T.J., Mah, C.S., Lawson, L.A., Martin, A.D., Fuller, D.D., Cleaver, B.D., Clement, N., Phillips, D., Islam, S., Dobjia, N., Byrne, B.J., Phase I/II trial of adeno-associated virus-mediated alpha-glucosidase gene therapy to the diaphragm for chronic respiratory failure in pompe disease: initial safety and ventilatory outcomes. Hum. Gene Ther. 24 (2013), 630–640.
27. Smith, B.K., Gabrielli, A., Davenport, P.W., Martin, A.D., Effect of training on inspiratory load compensation in weaned and unweaned mechanically ventilated ICU patients. Respir. Care 59 (2014), 22–31.
28. Smith, B.K., Corti, M., Martin, A.D., Fuller, D.D., Byrne, B.J., Altered activation of the diaphragm in late-onset Pompe disease. Respir. Physiol. Neurobiol. 222 (2016), 11–15.
29. Smith, B. K., Fuller, D.D., Martin, A.D., Lottenberg, L., Islam, S., Lawson, L.A., Onders, R.P., Byrne, B.J., 2016b. Diaphragm pacing as a rehabilitative tool for patients with Pompe disease who are ventilator-dependent: Case series. Phys. Ther. 96, 696–703.
30. Van den Hout, H., Reuser, A.J., Vulto, A.G., Loonen, M.C., Cromme-Dijkhuis, A., Van der Ploeg, A.T., Recombinant human alpha-glucosidase from rabbit milk in Pompe patients. Lancet 356 (2000), 397–398.
31. van den Hout, H.M., Hop, W., van Diggelen, O.P., Smeitink, J.A., Smit, G.P., Poll-The, B.T., Bakker, H.D., Loonen, M.C., de Klerk, J.B., Reuser, A.J., van der Ploeg, A.T., The natural course of infantile Pompe's disease: 20 original cases compared with 133 cases from the literature. Pediatrics 112 (2003), 332–340.
32. Van den Hout, J.M., Kamphoven, J.H., Winkel, L.P., Arts, W.F., De Klerk, J.B., Loonen, M.C., Vulto, A.G., Cromme-Dijkhuis, A., Weisglas-Kuperus, N., Hop, W., Van Hirtum, H., Van Diggelen, O.P., Boer, M., Kroos, M.A., Van Doorn, P.A., Van der Voort, E., Sibbles, B., Van Corven, E.J., Brakenhoff, J.P., Van Hove, J., Smeitink, J.A., de Jong, G., Reuser, A.J., Van der Ploeg, A.T., Long-term intravenous treatment of Pompe disease with recombinant human alpha-glucosidase from milk. Pediatrics 113 (2004), e448–e457.