Evolution of Muscular Oxygenation during a Walking Test in Pre-Term Children

Published:August 01, 2020DOI:https://doi.org/10.1016/j.jpeds.2020.07.082



      to explore measures of peripheral muscular oxygenation, coupled to gait characteristics, between premature and full-term children during a 6-minute walking test (6MWT).

      Study design

      Prepubescent children performed a 6MWT. During the test, changes in muscular oxyhaemoglobin (ΔHbO 2), deoxyhaemoglobin (ΔHHb) and total haemoglobin (ΔtHb) were measured with NIRS technology, positioned on subjects’ calves. Gait variables were monitored with an OPTOGAIT system.


      45 children (33 FT children and 12 PT children) participated in this study (mean age±SD: 4.9±0.7 and 4.6±0.9 years, respectively). Statistical analysis highlighted a decreased walking performance for PT children, with significantly lower walking distance ( P < .05) than children born FT (405.1±91.8m vs. 461.0±73.3m respectively, -9%). A concomitant increase of oxygen extraction (over ΔHHb time course) was observed from the third minute of the test (p<0.05). No statistically significant difference was found for other NIRS measures. Lastly, the analysis of gait variables highlighted a group effect for walking speed (p<0.05) and stride length (p<0.01).


      Premature children showed decreased walking performance and greater change in peripheral muscular oxygen extraction, associated with lower walking speed and stride length. This may point to a muscular maladjustment and reduced functional capacities for children born PT. These phenomena could be responsible for greater muscular fatigue.


      List of abreviations:

      6MWT ( 6-Minute Walking Test), ΔHbO2 ( Variation of Oxyhemoglobin), ΔHbTot ( Variation of Total Hemoglobin), ΔHHb ( Variation of Desoxyhemoglobin), BPD ( Bronchopulmonary Dysplasia), COPD ( Chronic Obstructive Pulmonary Disease), NIRS ( Near Infra-Red Spectroscopy)
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        • Narang I.
        Review series: What goes around, comes around: childhood influences on later lung health? Long-term follow-up of infants with lung disease of prematurity.
        Chron Respir Dis. 2010; 7: 259-269
        • O’Donnell D.E.
        Adult survivors of preterm birth. What spirometry conceals, exercise tests reveal.
        Ann Am Thorac Soc. déc. 2014; 11: 1606-1607
        • Kriemler S.
        • Keller H.
        • Saigal S.
        • Bar-Or O.
        Aerobic and lung performance in premature children with and without chronic lung disease of prematurity.
        Clin J Sport Med Off J Can Acad Sport Med. sept. 2005; 15: 349-355
        • Lovering A.T.
        • Elliott J.E.
        • Laurie S.S.
        • Beasley K.M.
        • Gust C.E.
        • Mangum T.S.
        • et al.
        Ventilatory and sensory responses in adult survivors of preterm birth and bronchopulmonary dysplasia with reduced exercise capacity.
        Ann Am Thorac Soc. déc. 2014; 11: 1528-1537
        • MacLean J.E.
        • DeHaan K.
        • Fuhr D.
        • Hariharan S.
        • Kamstra B.
        • Hendson L.
        • et al.
        Altered breathing mechanics and ventilatory response during exercise in children born extremely preterm.
        Thorax. nov. 2016; 71: 1012-1019
        • Maltais F.
        • Decramer M.
        • Casaburi R.
        • Barreiro E.
        • Burelle Y.
        • Debigaré R.
        • et al.
        An Official American Thoracic Society/European Respiratory Society Statement: Update on Limb Muscle Dysfunction in Chronic Obstructive Pulmonary Disease.
        Am J Respir Crit Care Med. mai. 2014; 189e15-62
        • Höller N.
        • Urlesberger B.
        • Mileder L.
        • Baik N.
        • Schwaberger B.
        • Pichler G.
        Peripheral Muscle Near-Infrared Spectroscopy in Neonates: Ready for Clinical Use? A Systematic Qualitative Review of the Literature.
        Neonatology. 2015; 108: 233-245
        • Allart E.
        • Olivier N.
        • Hovart H.
        • Thevenon A.
        • Tiffreau V.
        Evaluation of muscle oxygenation by near-infrared spectroscopy in patients with Becker muscular dystrophy.
        Neuromuscul Disord NMD. août. 2012; 22: 720-727
        • Moalla W.
        • Elloumi M.
        • Chamari K.
        • Dupont G.
        • Maingourd Y.
        • Tabka Z.
        • et al.
        Training effects on peripheral muscle oxygenation and performance in children with congenital heart diseases.
        Appl Physiol Nutr Metab Physiol Appl Nutr Metab. août. 2012; 37: 621-630
        • Adami A.
        • Cao R.
        • Porszasz J.
        • Casaburi R.
        • Rossiter H.B.
        Reproducibility of NIRS assessment of muscle oxidative capacity in smokers with and without COPD.
        Respir Physiol Neurobiol. 2017; 235: 18-26
        • Tsopanoglou S.P.
        • Davidson J.
        • Goulart A.L.
        • Barros MC. de M.
        • dos Santos A.M.N.
        Functional capacity during exercise in very-low-birth-weight premature children.
        Pediatr Pulmonol. janv. 2014; 49: 91-98
      1. Kutsuzawa T, Kurita D, Ikeuchi M. Oxygenation state of the calf muscle during the 6-min walk test in patients with COPD. Eur Respir J [Internet]. 1 sept 2015 [cité 19 mai 2020];46(suppl 59). Disponible sur: https://erj.ersjournals.com/content/46/suppl_59/PA2294

        • Boushel R.
        • Langberg H.
        • Olesen J.
        • Gonzales-Alonzo J.
        • Bülow J.
        • Kjaer M.
        Monitoring tissue oxygen availability with near infrared spectroscopy (NIRS) in health and disease.
        Scand J Med Sci Sports. août. 2001; 11: 213-222
        • Leclair E.
        • Borel B.
        • Baquet G.
        • Berthoin S.
        • Mucci P.
        • Thevenet D.
        • et al.
        Reproducibility of measurement of muscle deoxygenation in children during exercise.
        Pediatr Exerc Sci. mai. 2010; 22: 183-194
        • Singh S.J.
        • Puhan M.A.
        • Andrianopoulos V.
        • Hernandes N.A.
        • Mitchell K.E.
        • Hill C.J.
        • et al.
        An official systematic review of the European Respiratory Society/American Thoracic Society: measurement properties of field walking tests in chronic respiratory disease.
        Eur Respir J. déc. 2014; 44: 1447-1478
        • Holland A.E.
        • Spruit M.A.
        • Troosters T.
        • Puhan M.A.
        • Pepin V.
        • Saey D.
        • et al.
        An official European Respiratory Society/American Thoracic Society technical standard: field walking tests in chronic respiratory disease.
        Eur Respir J. déc. 2014; 44: 1428-1446
        • Lienhard K.
        • Schneider D.
        • Maffiuletti N.A.
        Validity of the Optogait photoelectric system for the assessment of spatiotemporal gait parameters.
        Med Eng Phys. avr. 2013; 35: 500-504
        • Edwards M.O.
        • Kotecha S.J.
        • Lowe J.
        • Watkins W.J.
        • Henderson A.J.
        • Kotecha S.
        Effect of preterm birth on exercise capacity: A systematic review and meta-analysis.
        Pediatr Pulmonol. mars. 2015; 50: 293-301
        • Moalla W.
        • Merzouk A.
        • Costes F.
        • Tabka Z.
        • Ahmaidi S.
        Muscle oxygenation and EMG activity during isometric exercise in children.
        J Sports Sci. nov. 2006; 24: 1195-1201
        • van Beekvelt M.C.P.
        • van Engelen B.G.M.
        • Wevers R.A.
        • Colier W.N.J.M.
        In vivo quantitative near-infrared spectroscopy in skeletal muscle during incremental isometric handgrip exercise.
        Clin Physiol Funct Imaging. mai. 2002; 22: 210-217
        • Murthy G.
        • Kahan N.J.
        • Hargens A.R.
        • Rempel D.M.
        Forearm muscle oxygenation decreases with low levels of voluntary contraction.
        J Orthop Res Off Publ Orthop Res Soc. juill. 1997; 15: 507-511
      2. DeLorey DS, Kowalchuk JM, Paterson DH. Relationship between pulmonary O2 uptake kinetics and muscle deoxygenation during moderate-intensity exercise. J Appl Physiol Bethesda Md 1985. juill 2003;95(1):113-120.

        • Lewandowski A.J.
        • Augustine D.
        • Lamata P.
        • Davis E.F.
        • Lazdam M.
        • Francis J.
        • et al.
        Preterm Heart in Adult Life: Cardiovascular Magnetic Resonance Reveals Distinct Differences in Left Ventricular Mass, Geometry, and Function.
        Circulation. 15 janv. 2013; 127: 197-206
        • Wenchich L.
        • Zeman J.
        • Hansíková H.
        • Plavka R.
        • Sperl W.
        • Houstek J.
        Mitochondrial energy metabolism in very premature neonates.
        Biol Neonate. 2002; 81: 229-235
        • Miura H.
        • McCully K.
        • Chance B.
        Application of Multiple NIRS Imaging Device to the Exercising Muscle Metabolism.
        Spectroscopy. 2003; 17: 549-558