VIEW Open Access Ultrasound and Non‑Ultrasound Imaging Techniques in the Assessment of Diaphragmatic Dysfunction Franco A
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Laghi Jr. et al. BMC Pulm Med (2021) 21:85 https://doi.org/10.1186/s12890-021-01441-6 REVIEW Open Access Ultrasound and non-ultrasound imaging techniques in the assessment of diaphragmatic dysfunction Franco A. Laghi Jr.1, Marina Saad2 and Hameeda Shaikh3,4* Abstract Diaphragm muscle dysfunction is increasingly recognized as an important element of several diseases including neuromuscular disease, chronic obstructive pulmonary disease and diaphragm dysfunction in critically ill patients. Functional evaluation of the diaphragm is challenging. Use of volitional maneuvers to test the diaphragm can be limited by patient efort. Non-volitional tests such as those using neuromuscular stimulation are technically complex, since the muscle itself is relatively inaccessible. As such, there is a growing interest in using imaging techniques to characterize diaphragm muscle dysfunction. Selecting the appropriate imaging technique for a given clinical sce- nario is a critical step in the evaluation of patients suspected of having diaphragm dysfunction. In this review, we aim to present a detailed analysis of evidence for the use of ultrasound and non-ultrasound imaging techniques in the assessment of diaphragm dysfunction. We highlight the utility of the qualitative information gathered by ultrasound imaging as a means to assess integrity, excursion, thickness, and thickening of the diaphragm. In contrast, quantitative ultrasound analysis of the diaphragm is marred by inherent limitations of this technique, and we provide a detailed examination of these limitations. We evaluate non-ultrasound imaging modalities that apply static techniques (chest radiograph, computerized tomography and magnetic resonance imaging), used to assess muscle position, shape and dimension. We also evaluate non-ultrasound imaging modalities that apply dynamic imaging (fuoroscopy and dynamic magnetic resonance imaging) to assess diaphragm motion. Finally, we critically review the application of each of these techniques in the clinical setting when diaphragm dysfunction is suspected. Keywords: Diaphragm dysfunction, Ultrasound imaging, Static imaging techniques, Dynamic imaging techniques, Phrenic nerve, Mechanical ventilation, Neuromuscular disorders Background or no respiratory symptoms [1]. In other patients, this Te diaphragm is the main muscle of respiration dur- compensation is associated with signifcant respiratory ing resting breathing [1]. When respiratory demands symptoms. Diaphragm dysfunction can cause alveolar are increased or diaphragm function is impaired, rib hypoventilation and, in the most severe cases, respira- cage muscles and expiratory muscles are progressively tory failure requiring mechanical ventilation [1, 2]. Te recruited [2]. In some patients with diaphragm dys- ultimate causes of diaphragmatic dysfunction can be function, this compensation is associated with minimal broadly grouped into three major categories: disorders of central nervous system or peripheral neurons, disorders of the neuromuscular junction and disorders of the con- *Correspondence: [email protected] tractile machinery of the diaphragm itself [3] (Table 1). 3 Division of Pulmonary and Critical Care Medicine, Hines Veterans Afairs Early diagnosis of diaphragmatic dysfunction is essential, Hospital (111N), 5th Avenue and Roosevelt Road, Hines, IL 60141, USA Full list of author information is available at the end of the article © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Laghi Jr. et al. BMC Pulm Med (2021) 21:85 Page 2 of 29 Table 1 Pathophysiological causes of diaphragmatic dysfunction Group Examples Neuronal disorders a) Disorders of CNS Poliomyelitis, ALS, multiple sclerosis, spinal cord injury b) Disorders of peripheral neurons Guillain–Barre syndrome, chronic infammatory demyelinating polyneuropathy, critical illness polyneuropa- thy, compression of the phrenic nerve by neighboring structures Disorders of the neuromuscular junction Myasthenia gravis, Lambert-Eaton syndrome, botulism, organophosphates Disorders of the muscle Muscular dystrophies, critical-illness myopathy, acid maltase defciency (Pompe disease), dermatomyositis CNS central nervous system, ALS amyotrophic lateral sclerosis because it may be responsive to therapeutic intervention investigators reported a close correlation between dia- [4–7]. phragm thickness measured in cadavers using ultrasound A number of static and dynamic imaging techniques imaging and thickness measured with a ruler (Fig. 1). are used in the evaluation of patients suspected of dia- Since the seminal work of Wait et al. [18], investigators phragm dysfunction [8]. Static imaging techniques are have published a growing number of studies on the use used to assess the position, shape and dimensions of the of ultrasonography to monitor the thickness of the dia- diaphragm and include chest radiography [9], brightness phragm in the zone of apposition, the motion of the mode (B-mode) ultrasound [10, 11], computed tomog- dome and to estimate diaphragm strength and recruit- raphy (CT) [12], and static magnetic resonance imag- ment during voluntary contractions [19, 20]. ing (MRI) [13]. Dynamic imaging techniques are used to assess diaphragm motion in one or more directions. Tis Ultrasound measurement of diaphragm thickness (zone group of imaging techniques include fuoroscopy [14], of apposition) motion mode (M-mode) ultrasonography [10, 11, 15], Operators use linear ultrasound probes to measure dia- and dynamic MRI [16]. phragm thickness [15] (Fig. 2). Tese probes use high Te purpose of this review is to present the accumu- frequency ultrasound waves (7–18 Hz) to create high lated knowledge on imaging techniques used in the resolution images of structures near the body surface evaluation of diaphragm dysfunction. A MEDLINE [15]. To measure diaphragm thickness, operators place search of articles published between 2010 and 2020 was the ultrasound probe longitudinally parallel to the long undertaken. Searches of the bibliographies of articles axis of the body, usually between the eighth to tenth resulted in several additional articles and book chapters. Information was selected on the basis of scientifc qual- ity and potential relevance to patients sufering from a pulmonary disease or a disorder requiring admission to an intensive care unit; in all, a total of 128 sources were included in this review. In this review we will frst discuss ultrasound imaging techniques and then non-ultrasound imaging techniques. We will then discuss the clinical applications of these techniques. Finally, we will provide a critical appraisal of the limitations of ultrasound and non-ultrasound imag- ing in the evaluation of diaphragmatic dysfunction and considerations about future directions. Ultrasound imaging of the diaphragm Diaphragm ultrasonography was frst described in the late 1960s as a means to determine position and size of Fig. 1 Relationship of diaphragm thickness measured in situ in 10 supra- and subphrenic mass lesions, and to assess the human cadavers by ultrasound and in vitro by a ruler. Ultrasound motion and contour of the diaphragm [17]. Two decades measurements of diaphragm thickness in situ are as accurate as measurements in vitro with a ruler. Reproduced with permission later, Wait et al. [18] developed a technique to measure from The American Physiological Society: Wait et al. J Appl Physiol diaphragm thickness based on ultrasonography. Te 1989;67(4):1560–1568 Laghi Jr. et al. BMC Pulm Med (2021) 21:85 Page 3 of 29 Fig. 2 Ultrasound image of the zone of apposition of the diaphragm. In brightness-mode (B-mode; left panel), the diaphragm appears as a three-layer structure. In motion-mode (M-mode; right panel), the diaphragm is thinnest at end-exhalation and thickest at end-inhalation; stronger diaphragmatic inspiratory eforts are associated with greater tidal thickening of the diaphragm. Reproduced with permission from The American Association for Respiratory Care: Shaikh et al. Respir Care 2019;64:1600–2. The entirety of both images was obtained by Dr. Shaikh intercostal space [21, 22], at the anterior axillary line [15] intercostal space: in a study of 150 healthy subjects [26] or midway between the anterior- and mid-axillary lines investigators reported as much as a 6-mm change in rest- [23]. Te costo-phrenic sinus [24] is identifed as the ing thickness from one intercostal space to another. transition between lung and liver (right) or between lung Diaphragm thickness while healthy subjects rest at and spleen