Ninane V.

Redolfi S.

Similowski T.

Straus C.

English

Archivio istituzionale della ricerca - Università di Cagliari

LETTER TO THE EDITORPostural lung volume reduction,expiratory flow limitation, andorthopnoea in diaphragmaticweakness: PreliminaryobservationsPatients with diaphragmatic weakness complain of dyspnoeawhen lying supine, bending forward, swimming, or bathing.The corresponding mechanisms remain unclear. Septatingthe coelomic cavity, the diaphragm protects the lungs fromabdominal compression.1 Diaphragm paralysis and atrophyabolish this protection. This reduces lung volume, particu-larly during postural changes because the transferredabdominal weight exerts an expiratory action on the unpro-tected lungs1. Lung compliance and upper airway collapsibil-ity depend on diaphragm activity and their posturaldeterioration could contribute to orthopnoea throughincreased work of breathing.2,3 In addition, through theassociated lung volume reduction, diaphragm dysfunctioncould lead to expiratory flow limitation (inability to increaseexpiratory flow when expiratory driving pressure augments).Expiratory flow limitation is associated with dyspnoeabecause the associated changes in operating lung volumesincrease the inspiratory muscles burden.4 Postural expira-tory flow limitation is associated with orthopnoea in chronicobstructive pulmonary disease (COPD), left heart failure(LHF), and morbid obesity.4,5 We therefore hypothesisedthat diaphragm weakness could be associated with a pos-tural reduction in operating lung volume (reduction in expi-ratory reserve) hence expiratory flow limitation andorthopnoea.The study was approved by the institutional reviewboard of the French society for respiratory medicine (deci-sion “CEPRO 2022-017”, April 2, 2022). Patients providedwritten consent. Inclusion criteria were: age over 18; dia-phragm weakness (oesophageal pressure twitch response tobilateral phrenic stimulation —Poes,tw—< 11 cmH2O-6).Non-inclusion criteria were: obstructive ventilatory defect;body mass index over 30 kg.m2; abdominal parietaldefects. Dyspnoea was evaluated using a 10-cm visual ana-logue scale (VAS; 0, no difficulty; 10, worst imaginable).Orthopnoea was defined by an increase in VAS (∆-VAS) of1 cm or more after lying supine. Sitting and supine vitalcapacity (VC), inspiratory capacity (IC), and expiratoryreserve volume (ERV) were obtained using standardspirometry. Expiratory flow limitation was looked for bycomparing resting breathing flow-volume loops (naturalFVL) with FVLs in response to an increase in the alveolar-atmospheric gradient (stimulated FVL) determined by:1) the application of a 5 cmH2O negative expiratory pres-sure at the mouth (Medisoft Expair, Belgium); 2) manualabdominal compression.7,8 Expiratory flow limitation wasidentified when the stimulated FVL was partially or entirelysuperimposed on the natural FVL. Data are summarised asmedian [min-max]. Patients with and without expiratoryflow limitation were compared using Mann-Whitney U testand Fischer’s exact text. Statistical significance was set atp <0.05.Thirteen patients were studied. Their characteristics aredescribed in Table 1. ERV markedly decreased when supine(35% [22;70]), the fall exceeding 20% in all patients.Supine changes in VC were modest and inconsistent (- 8%[3; 32], falls exceeding 15% in only four patients and 20%in only two). The same was true for IC (1% [0.21; +0.19]).Supine expiratory flow limitation occurred in 8 cases (exam-ple in Fig. 1A and 1B; perfect concordance between negativeexpiratory pressure and manual abdominal compression).These 8 patients experienced orthopnoea (∆VAS=3. [1,6;6,8]). None of the remaining five patients had expiratoryflow limitation, but one reported orthopnoea. The associa-tion of expiratory flow limitation with orthopnoea was sta-tistically significant (p = 0.007). There was no discernibledifference between uni- or bilateral diaphragm dysfunction.Two patients with expiratory flow limitation were studiedthree months after diaphragm plication: VC and ERVimproved by about 15%, no supine fall in ERV were observedanymore, and both orthopnoea and expiratory flow limita-tion had disappeared (Fig. 1C).As hypothesised, lying supine was consistently associatedwith a marked ERV decrease, attesting to an expiratoryeffect of the posture-related cephalad shift of the abdomi-nal content in patients with diaphragmatic weakness. Expi-ratory flow limitation did not occur consistently, but itsoccurrence bore a statistically significant relationship withorthopnoea. We acknowledge that this is a small explor-atory study and that we did not engage in a comprehensivepathophysiological dissection of the mechanisms of orthop-noea. Nevertheless, from our observations we propose thatpostural expiratory flow limitation contributes to dia-phragm weakness-related orthopnoea. This closely resem-bles LHF, COPD, and massive obesity.4,5 In the two patientshttps://doi.org/10.1016/j.pulmoe.2023.08.0072531-0437/© 2023 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L.U. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).Pulmonology 30 (2024) 188191www.journalpulmonology.orgTable 1 Characteristics of the patients.Patient Sex Age BMI sitting VC sitting IC sitting ERV MIP SNIP Poes.tw EFL uni/bilateral aetiologyyears kg.m2 % pred % pred % pred % pred % pred cmH201 F 65 26 59 53 72 70 44 2 yes unilateral unidentified2 M 46 23.6 57 70 34 40  7 yes unilateral cervical arthrosis*3 F 45 24.7 33 34 9 64 68 6 yes bilateral amyotrophic lateral sclerosis4 M 32 27.7 96 100 88 88 82 8 yes unilateral cervical arthrosis*5 F 49 15.6 52 72 17 82 85 3 yes unilateral unidentified6 F 83 20.8 54 74 59 62 60 4 yes unilateral unidentified7 M 44 27.5 104 136 57 58 64 6 yes unilateral unidentified8 M 61 30.1 95 90 93 51 50 7.5 yes unilateral unidentified. suspected Par-sonage Turner9 M 61 22.5 70 76 85 67 42 2.5 no bilateral amyotrophic lateral sclerosis10 F 51 30.5 77 99 30 90 94 6.5 no bilateral cervical myelopathy11 M 61 29.4 66 68 77 47  5 no bilateral post cardiac surgery12 M 61 21.4 69 85 50 34 46 4 no unilateral post cardiac surgery13 F 33 31.6 24 29 26 80 78 8 no unilateral Pompe diseasemedian  51 26.0 66.0 74.0 57.0 64 64 6.0   Minimum  32 15.6 33.0 29.0 9.0 34 42 2.0   Maximum  83 31.6 104.0 136.0 93.0 90 94 8.0   BMI. body mass index; VC. vital capacity; IC. inspiratory capacity; ERV. expiratory reserve volume; MIP. maximal inspiratory pressure.SNIP. sniff nasal inspiratory pressure; Poes.tw. twitch oesophageal pressure; EFL. expiratory flow limitation.NB: room air pulsed transcutaneous haemoglobin oxygen saturation  95% il all cases.* with neuroforaminal stenosis.189Pulmonology30(2024)188191with diaphragm plication, the supine fall in ERV disap-peared as did expiratory flow limitation and orthopnoea(Fig. 1C). In conclusion, and of clinical relevance, our datajustify further investigation of the diagnostic value of pos-tural changes in ERV in to screen for diaphragm weaknessand its comparison with the more traditional posturalchanges in VC that are not very sensitive. Our data also jus-tify further investigation of the value of postural expiratoryflow limitation when discussing diaphragm plication, anintervention of which the indications are not codified andthe results difficult to anticipate: the possibility of predict-ing the symptomatic results of diaphragm plication wouldalso be of clinical relevance.Data management and sharingAll data will be made available by the authors upon reason-able request.Declaration of generative AI in scientific writingNo generative AI was used for the present manuscript.Previous presentation at research meetingsNone.Authors’ contributionsStefania REDOLFI: conception and design; data acquisitionand analysis; drafting; final approval; Vincent NINANE: con-ception and design; data analysis; final approval; ChristianSTRAUS: conception and design; data analysis; finalapproval; Thomas SIMILOWSKI conception and design; dataacquisition and analysis; drafting; final approval.FundingThis research received no specific grant from any fundingagency in the public, commercial, or not-for-profit sectors.Conflicts of interestThe authors declare that they have no known competingfinancial interests or personal relationships that could haveappeared to influence the work reported in this paper.AcknowledgementThis study is dedicated to the memory of Pr Joseph Milic-Emili, 1931-2022.References1. Perry SF, Similowski T, Klein W, Codd JR. The evolutionary originof the mammalian diaphragm. Respir Physiol Neurobiol.2010;171:116.2. Takeda S, Nakahara K, Fujii Y, Matsumura A, Minami M, MatsudaH. Effects of diaphragmatic plication on respiratory mechanics indogs with unilateral and bilateral phrenic nerve paralyses. Chest.1995;107:798804.3. Hillman DR, Walsh JH, Maddison KJ, Platt PR, Schwartz AR, East-wood PR. The effect of diaphragm contraction on upper airwaycollapsibility. J Appl Physiol (1985). 2013;115:33745.4. Tantucci C. Expiratory flow limitation definition, mechanisms,methods, and significance. Pulm Med. 2013;2013:749860.Fig. 1 Flow-volume curves recorded during tidal breathing (blue lines; inspiration bottom, expiration top) and in response to man-ual abdominal compression (black lines) in one typical patient, in the sitting posture (A), the supine posture (B), and the supine pos-ture three months after surgical diaphragm plication (C). The red arrows at the top of the panels denote the start and the end of theabdominal compression. The red arrows superimposed on the tidal flow volume curves indicate end-expiratory lung volume (EELV).Panel B shows expiratory flow limitation, with the manual compression-induced expiratory flow not exceeding the spontaneous expi-ratory flow during most of the expiration. Expiratory flow limitation does not occur in A and C. Note that the shape of the tidal flow-volume curve is different in B, with a marked downward expiratory slope that is not seen in A and C.190S. Redolfi, C. Straus, V. Ninane et al.5. Duguet A, Tantucci C, Lozinguez O, et al. Expiratory flow limita-tion as a determinant of orthopnoea in acute left heart failure. JAm Coll Cardiol. 2000;35:690700.6. Laveneziana P, Albuquerque A, Aliverti A, et al. ERS statement onrespiratory muscle testing at rest and during exercise. Eur RespirJ. 2019;53:1801214.7. Koulouris NG, Valta P, Lavoie A, et al. A simple method to detectexpiratory flow limitation during spontaneous breathing. EurRespir J. 1995;8:30613.8. Ninane V, Leduc D, Kafi SA, Nasser M, Houa M, Sergysels R. Detec-tion of expiratory flow limitation by manual compression of theabdominal wall. Am J Respir Crit Care Med. 2001;163:132630.S. Redolfia,b, C. Strausc,d, V. Ninanee, T. Similowskid,f,*a AP-HP, Groupe Hospitalier APHP-Sorbonne Universite,Hôpital Pitie-Salpêtriere, Service des Pathologies duSommeil (Departement R3S), F-75013 Paris, Franceb Dipartimento di Scienze Mediche e Sanita Pubblica,Universita di Cagliari, 09134 Cagliari, Italyc AP-HP, Groupe Hospitalier APHP-Sorbonne Universite,Hôpital Pitie-Salpêtriere, Service des ExplorationsFonctionnelles de la Respiration, de l’Exercice et de laDyspnee (Departement R3S), F-75013 Paris, Franced Sorbonne Universite, Inserm, UMRS 1158, F-75013 Paris,Francee Service de pneumologie, Hôpital Universitaire Saint-Pierre, Universite Libre de Bruxelles, Brussels, Belgiumf AP-HP, Groupe Hospitalier APHP-Sorbonne Universite,Hôpital Pitie-Salpêtriere, Departement R3S, F-75013 Paris,France* Corresponding author at: Departement R3S (Respiration,Reanimation, Readaptation respiratoire, Sommeil), HôpitalPitie-Salpêtriere, 47-83, Bd de l’Hôpital, 75651, Paris Cedex13, France.E-mail address: thomas.similowski@upmc.fr (T. Similowski).Received 9 July 2023; Accepted 3 August 2023Available online 22 September 2023191Pulmonology 30 (2024) 188191

Postural lung volume reduction, expiratory flow limitation, and orthopnoea in diaphragmatic weakness: Preliminary observations

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Postural lung volume reduction, expiratory flow limitation, and orthopnoea in diaphragmatic weakness: Preliminary observations

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