Short communicationCartography of human diaphragmatic innervation: Preliminary data
Introduction
Embryologically, the mammalian diaphragm originates in cervical somites. During development and together with the lungs, it migrates caudally to its ultimate location in the thorax. This accounts for the cervical origin of its innervation. Indeed, the phrenic nerve which provides the diaphragmatic motor innervation arises from cervical spinal segments C3–C7, depending on species. The corresponding somatotopic organisation—namely how the cervical roots distribute to the anterior, lateral and posterior regions of the diaphragm—has been described in the rat (C4–C6 in Gottschall and Gruber, 1977), the rabbit (C4–C6 in Marie et al., 1997b, Marie et al., 1999), the cat (C4–C6 in Sant’Ambrogio et al., 1963) and the dog (C5–C7 in De Troyer et al., 1982, Marie et al., 2006). In humans, abundant anatomical data indicate that the phrenic nerve is mainly constituted from a C4 component, with variable contributions of C3 and C5 (Hovelacque, 1927, Rajanna, 1947, Hidayet et al., 1974). How each of these roots innervates the human diaphragm topographically and quantitatively has not been described. This distribution can have both physiological and clinical implications, for example, regarding the use of cervical roots for reinnervation purposes or the consequences and management of spinal cord injuries. In this frame, we herein describe the diaphragm response to electrical stimulation of the C3, C4 and C5 cervical roots in three patients undergoing surgical laryngeal reinnervation.
Section snippets
Patients
Three female patients (39, 42 and 45 years of age) were studied. They all had bilateral laryngeal paralysis in the adductory position diagnosed by laryngoscopy and laryngeal electromyography, and had been enrolled for this reason in a protocol of laryngeal reinnervation with an upper phrenic root (details on ClinicalTrials.gov, NCT00213616). The diaphragm innervation cartography was part of this study and as such had been approved by the appropriate legal and ethical body (Comité de Protection
Preoperative observations
Phrenic nerve conduction times were in the normal range for the technique used (5.5 and 5.3 ms on the right and left side respectively in patient #1, 5.3 and 5.6 ms in patient #2, 5.7 and 5.4 ms in patient #3) (Similowski et al., 1997, American Thoracic Society and European Respiratory Society, 2002). At a given recording site, the amplitude of the electromyographic response to cervical magnetic stimulation was consistently symmetrical. Transdiaphragmatic pressures were also in the normal range
Discussion
This study is seemingly the first to provide human data about the diaphragmatic distribution of the cervical roots that contribute to the phrenic nerve. Our observations confirm the anatomically and clinically well-known dominance of C4. In addition, and even though generalisation is precluded by the very small number of patients, they suggest that the C5 contribution to the phrenic nerve can be of importance.
From a methodological point of view, we acknowledge that intradiaphragmatic recordings
Funding
The study was supported principally by grant 99-141-HP of the “Programme Hospitalier de Recherche Clinique (PHRC) Régional”, Direction de la Recheche Clinique, Rouen (Eric Verin, Jean-Paul Marie). It was also supported by grant DRC98075 from the Programme Hospitalier de Recherche Clinique National of the French Ministry of Health (Thomas Similowski).
Conflicts of interest
None declared.
Acknowledgements
The authors are grateful to Paul Robinson for his help with English style and grammar and for proofreading the manuscript.
References (19)
Phrenic nerve stimulation in patients with spinal cord injury
Respir. Physiol. Neurobiol.
(2009)- et al.
Surgical anatomy of the accessory phrenic nerve
Ann. Thorac. Surg.
(2006) - et al.
Diaphragmatic effects of selective resection of the upper phrenic nerve root in dogs
Respir. Physiol. Neurobiol.
(2006) - et al.
Selective resection of the phrenic nerve roots in rabbits. Part I. Cartography of the residual innervation
Respir. Physiol.
(1997) - et al.
Selective resection of the phrenic nerve roots in rabbits. Part II. Respiratory effects
Respir. Physiol.
(1997) - et al.
ATS/ERS statement on respiratory muscle testing
Am. J. Respir. Crit. Care Med.
(2002) - et al.
Action of costal and crural parts of the diaphragm on the rib cage in dog
J. Appl. Physiol.
(1982) Spinal and supraspinal factors in human muscle fatigue
Physiol. Rev.
(2001)- et al.
The accessory phrenic nerve in the rat
Anat. Embryol. (Berl.)
(1977)
Cited by (15)
What are the perspectives for ventilated tetraplegics? A French retrospective study of 108 patients with cervical spinal cord injury
2015, Annals of Physical and Rehabilitation MedicineCitation Excerpt :Patients presenting with high spinal cord injury can also present with severe ventilatory disorders; in this population, the latter constitutes the second most frequent cause of mortality during the first year following the trauma (28% of deaths) [7], and the first cause of mortality subsequent to the first year (31% of deaths) [8]. Respiratory failure is connected with damage to motor control of the diaphragm [9], of which the innervation by the phrenic nerve essentially comes from C4, with variable contributions from C3 and C5 [10]. The proportion of tetraplegic patients relying on a ventilator is correspondingly higher and higher.
The evolution of laryngeal reinnervation, the current state of science and thoughts for future treatments
2014, Journal of VoiceCitation Excerpt :To avoid this, a unilateral nerve root would be taken and a cable graft used to innervate both PCA abductor muscles. A human study showed that the phrenic nerve arises mainly from the C4 nerve root with variable C3 and C5 contributions.25 Stimulation of each root showed that C4 was the main innervation to the diaphragm but that C5 can be of importance with stimulated pressure responses from the diaphragm almost equal to those produced from C4.
Novel role for non-invasive neuromodulation techniques in central respiratory dysfunction
2023, Frontiers in NeuroscienceNerve Reconstruction
2022, Textbook of Surgery of Larynx and TracheaBilateral Selective Laryngeal Reinnervation for Bilateral Vocal Fold Paralysis in Children
2020, JAMA Otolaryngology - Head and Neck SurgerySurgical reinnervation
2017, Neurolaryngology