The review was according to the PRISMA 2020 flow diagram (Figure 1 and Supplementary material 3). We intended to identify studies measuring respiratory muscles in healthy and patients by ultrasonography. Based on the suggestions of thoracic ultrasound from European Respiratory Society Statement (Laursen et al., 2021) and previous review on ultrasonography measurement (Sferrazza Papa et al., 2016), we chose studies based on the following criteria: (1) Study subjects were healthy or patients with respiratory muscle disorders for various causes, the subjects included in the part of the clinical application were stroke patients. (2) The ultrasonography evaluation of the respiratory muscle was clearly described with integrated protocol, the ultrasound equipment, experience of the operator, probe frequency selection, subject’s measurement position, selection of measuring points/ultrasound probe placement position, respiratory status during measurement, and whether the subject cooperated, and respiratory muscle’s values were recorded. (3) All included studies were published in English with full text (English articles that were not published in full text were removed), including original studies and clinical trials.

We searched articles published in the MEDLINE, Web of Science, and PubMed databases with no date restrictions up to 19 November 2022 (Supplementary material 1). The following keywords were used: Respiratory muscle ultrasonography-related words: ultrasonography, ultrasound, echotomography, sonography, echography, diaphragm, respiratory muscles, ventilatory muscles, and intercostal muscles based on title, abstract, and MeSH terms, and trapezius, sternocleidomastoid muscles, scalene muscles, parasternal intercostal muscle, inspiratory muscle, and expiratory muscle based on title and abstract. Stroke-related words were stroke, hemiplegia, cerebrovascular, CVA, apoplexy, vascular, brain, cerebral, intracerebral, hemorrhage, infarct, and ischemia based on title, abstract, and MeSH terms. The search strategy was created based on the PICO strategy: P (patient)—adults (healthy or diseases); I (intervention)—ultrasonography of the respiratory muscles (e.g., diaphragm, extra-diaphragmatic inspiratory muscles, abdominal muscles); C (comparator)—none; O (outcomes)—methodology and reference value.

Two review authors independently read the titles and abstracts of all literatures searched by the databases. Unified standards were used to extract relevant information from the full text of articles that met the inclusions. Data were extracted including participant demographics, ultrasonography evaluation protocol, subject population, reference values, etc.

The human inspiratory muscles in the neck include the scalene and sternomastoid. These muscles have similar respiratory actions on the chest wall and cause cranial displacement of the sternum and ribcage (Hudson et al., 2007). The human scalene are obligatory inspiratory muscles that have a greater mechanical advantage than sternomastoid. Lee et al. (2016) found that stretching of the scalene muscles improved vital capacity. Several studies used computed tomographic scan images to measure the changes in muscle length, muscle mass and size of the sternocleidomastoid muscle (Peche et al., 1996; Legrand et al., 2003).

One study evaluated the reliability of shear-wave elastography (SWE) to assess the anterior and middle scalene muscles in healthy adult subjects. Ultrasound examinations of the scalene muscles were performed by an L18–4 MHz linear-array transducer. The ultrasound transducer was placed just lateral to the thyroid lobe (Bedewi et al., 2021). However, the limitations of this study were the small sample size, and the lack of comparison with pathological tissue. Several studies used B mode linear probe of ultrasonography with frequency of 7–11 or 8.5–10.0 MHz for imaging of the trapezius (Adigozali et al., 2016; Kisilewicz et al., 2020). Subjects were asked to sit on the chair while they were in an upright and relaxed position (Adigozali et al., 2016). In order to measure the thickness and SWE of the trapezius, the position of the ultrasound probe was generally chosen the midpoint of the spinous process of 7th cervical vertebra and acromion process of right scapula were determined by palpation. However, due to the peculiarities of anatomy and the limitations of ultrasound technology, there were few ultrasound studies on the scalene, sternocleidomastoid muscles and the trapezius.

The expiratory muscles include the abdominal wall muscles (transversus abdominis muscle (TrA), internal oblique muscle (IO), external oblique muscle (EO), and rectus abdominis muscle (RA)), and some of the rib cage ones (e.g., the internal intercostal muscles and the triangularis sterni muscle) (De Troyer et al., 1998; Wilson et al., 2001; De Troyer et al., 2005; De Troyer and Boriek, 2011). During tidal breathing, the expiratory muscles are largely inactive (Shi et al., 2019), although the transversus abdominis muscle may occasionally show some activity during quiet breathing (De Troyer et al., 1990). Previous study has shown that transversus abdominis has an important role in posture (Belavý et al., 2017). The contraction of the transversus abdominis muscle with the other muscles of the abdominal cavity has also been shown to increase intra-abdominal pressure (Hodges and Gandevia, 2000). Activation of the expiratory muscles during breathing occurs when the load imposed on the inspiratory muscle increases (Shi et al., 2019). In the presence of an imbalance between inspiratory muscle load and capacity, the abdominal wall muscles are recruited during expiration in a fixed hierarchy (Aliverti et al., 1997; Parthasarathy et al., 2007): initially, the transversus abdominis muscle, followed by the internal oblique muscle and the external oblique muscle, and finally the rectus abdominis muscle (Abe et al., 1996; Suzuki et al., 1999). Abdominal ultrasound allows direct visualization of the three layers of the abdominal wall muscles (Misuri et al., 1997; McMeeken et al., 2004; Rankin et al., 2006; Tahan et al., 2016). In healthy subjects, the thickness of individual abdominal wall muscles follows a certain pattern: transversus abdominis < external oblique < internal oblique < rectus abdominis (Tahan et al., 2016).

Expiratory muscle thickness measurement (Table 3): Using 7.5 or 10–15 MHz linear probe in B-mode condition positioned perpendicular to the abdominal wall. Measurements were performed with the subjects in a supine or semi-recumbent position with knees bent and the hips at 45°. To visualize the rectus abdominis muscle, the transducer is positioned in a transverse orientation approximately 2–3 cm above the umbilicus and 2–3 cm lateral from the midline. The external oblique, internal oblique, and transversus abdominis muscles can be identified as three parallel layers, usually at the anterior axillary line, midway between the inferior border of the rib cage and the iliac crest. Several studies measured rectus abdominis at 3 cm or 4 cm lateral to the umbilicus; the external oblique, internal oblique, and transverse abdominis were measured at 2.5 cm anterior to the mid-axillary line and at the midpoint between the inferior rib and iliac crest. The pressure applied to the probe should be kept to a minimum to prevent compression of the abdominal wall as this may alter the shape/thickness of the underlying muscles. Abdominal muscle thickness was performed at the end of a relaxed expiration or at end-inspiration. Thickening fraction of the expiratory abdominal muscles (TFabd) can be calculated as the magnitude of thickness increase during expiration. Change in thickness determined the thickening fraction of the expiratory abdominal muscles (TFadb) as follows: TFadb = (end-expiratory thickness − end-inspiratory thickness)/end-inspiratory thickness × 100% (Tuinman et al., 2020).

To be useful, ultrasound measures should be reliable and with good reproducibility, which means that they are stable over time, have minimal variability, and have enough sensitivity to detect clinically important changes (Lexell and Downham, 2005). There were many studies on the feasibility and reliability of the diaphragmatic ultrasound measurements (Baldwin et al., 2011; Goligher et al., 2015). Ultrasonographic technique of diaphragm was previously reported to be reliable, with high intra-class correlation coefficient for intra-rater and inter-rater reliability (Gottesman and McCool, 1997; Boussuges et al., 2009). Diaphragm motion depend on the position of the subject in the study (Sarwal et al., 2013). The supine position is preferred, because there is less overall variability, less side-to-side variability, and greater reproducibility (Gerscovich et al., 2001). Baldwin et al. (2011) also found that ultrasound technique has good reliability in recumbent positions. In addition, the relationship between inspired volume and diaphragmatic motion was found to be linear (Houston et al., 1994).

On the contrary, very few studies have applied ultrasound to evaluate the extra-diaphragmatic inspiratory muscles. Parasternal intercostal muscle ultrasound may be a useful tool in the evaluation of the respiratory muscle in future studies (Tuinman et al., 2020). Dres et al. (2020) have proposed a technique to measure the parasternal intercostal muscle by ultrasonography, while their results need to be confirmed in a larger number of patients (Vivier and Mekontso Dessap, 2020). Intercostal muscle ultrasound offers a repeatable and radiation-free alternative, however requires validation. Wallbridge et al. (2018) found that the inter-rater reliability was not as strong for thickness, particularly in the third intercostal spaces bilaterally. The results of the research demonstrated that real time ultrasonography was a reliable method for measurement of upper trapezius (Adigozali et al., 2016). Other extra-diaphragmatic inspiratory muscles, such as the scalene muscles and sternocleidomastoid muscles, requires further study on their ultrasound approach, reliability, and reproducibility.

The measurement of abdominal wall muscles’ thickness was feasible in almost all healthy subjects and patients. A large number of studies evaluated the reproducibility of ultrasound imaging measures of abdominal muscle activity (McMeeken et al., 2004; English et al., 2012). Reliability in the measurement of abdominal muscle thickness was assessed in several studies and their results indicated an excellent inter-and intra-rater reproducibility in measuring the muscle thickness of these muscles (Ota et al., 2012; Shi et al., 2021).

The operator skills, technical aspects are related to ultrasound physics, and patient characteristics, e.g., probe orientation difficulties, the small muscles, muscle edema, and the pressure of the transducer and manipulator’s hand on the wall can all affect measurements (Tuinman et al., 2020; Vivier and Mekontso Dessap, 2020). Furthermore, the spatial axial resolution of the probe plays a critical role. Comparing individual patient results should be done with a degree of caution and only after adequate training (Tuinman et al., 2020).

Previous studies have some methods to reduce variability, such as the same normalized position of the subject and the exact position of the transducer were maintained during the measurement, use the minimum amount of pressure needed to get a clear image while preventing pressure that could alter the shape or thickness of the muscle (Tuinman et al., 2020), the same observer for three different cycles of measurement, and a unified standard for measurement software, etc. (Liu et al., 2022).

The risk of selection, performance, detection, and reporting bias in the included studies are specified in Table 4.

The human diaphragm represents one of the muscles that are controlled by an automatic as well as voluntary motor system (Nakayama et al., 2004). It is thought that bilateral hemi-diaphragms are controlled by the contralateral primary motor cortex and, thus, in the presence of paralysis, the diaphragm is also affected on the same side as the paralysis (Aminoff and Sears, 1971; Cohen et al., 1994). The etiology of the paralysis is multiple (Gerscovich et al., 2001). Central nervous system disease, including brain infarction, may impair diaphragmatic motion. Because ultrasonography can distinguish a functioning from a nonfunctioning diaphragm, it can be used to diagnose both unilateral and bilateral diaphragmatic paralysis and to monitor recovery of the paralyzed diaphragm (Gottesman and McCool, 1997; Summerhill et al., 2008). Respiratory exercises could contribute to the well-being of the stroke patients and this contribution could be followed up by diaphragm ultrasound (Kılıçoğlu et al., 2022).

Hemiplegic side of the diaphragm had reduced thickness and motion during voluntary inspiration on the same side of the body paralysis in patients with stroke (Laroche et al., 1988; Kim et al., 2017) and this finding was not seen during quiet breathing (Cohen et al., 1994). Our results of previous study were consistent with (Liu et al., 2022). However, there was controversy about the function of the hemiplegic side and non-hemiplegic side of the diaphragm after stroke. Some researchers showed that the motion of the diaphragm on the hemiplegic side decreases after stroke, and the contralateral showed a larger excursion compensatively (Cohen et al., 1994). However, Houston et al. (1995) found bilaterally decreased volitive diaphragmatic motion in acute cerebral infarction. Recent studies have found that the thickness and motion of the bilateral diaphragm in stroke patients were decreased (Caleffi-Pereira et al., 2018), while diaphragmatic dysfunction was more severe on the hemiplegic side (Catalá-Ripoll et al., 2020). In view of this, we reviewed the diaphragm thickness in hemiplegic patients after stroke at the subacute stage (almost within 1–6 months from the onset) with ultrasound in the literature, as shown in Figure 2. In most of the studies, the thickness of the diaphragm on the hemiplegic side of stroke patients is lower than that on the non-hemiplegic side, no matter at the end of inspiration or end of expiration (Supplementary material 2).

The function of hemiplegic expiratory muscles may be affected in stroke patients. It is therefore important to determine the quantitative and qualitative changes in abdominal muscles in stroke survivors. The hemiplegic side has been found to exhibit negative changes in abdominal muscle quantity and quality compared with the non-hemiplegic side or healthy controls (Monjo et al., 2022). One study has shown that the TrA on the hemiplegic side was 16% lower in the stroke patients compared to the matched side in the healthy people (Marsden et al., 2013). However, Kelli et al. (2020) found that bilateral TrA thickness decreased in the hemiplegia patients, suggesting muscle atrophy on both sides of the trunk. Kim et al. (2020) revealed that contractility of RA and EO at the paretic side was significantly lower than at the non-paretic side, while there were no significant difference between non-paretic and paretic sides at rest. Monjo et al. (2018) indicated that changes on the hemiplegic side in stroke survivors might not occur in the abdominal muscles. Regarding the reliability of ultrasound measurements, studies have shown that ultrasound is considered a reliable method for measuring muscle thickness in acute stroke patients (English et al., 2012). We summarized the thickness of abdominal respiratory muscles in hemiplegic patients after stroke in the literature, as shown in Figure 3. In the studies included, the average post-stroke duration of the expiratory muscles-related patients with hemiplegia ranged from months to years. Due to a large duration span, there was a lack of evaluation of possible bias. Consequently, we indicated reference numbers of different studies on the abscissa replaced the average duration of post-stroke in Figure 3. For IO and RA, two of three studies indicated that the thickness of the hemiplegic side of stroke patients was lower than that of the non-hemiplegia side, and one study found the opposite conclusion. For TrA, most studies showed that the thickness on the hemiplegic side was lower than that on the non-hemiplegia side; while for EO, all three studies showed that the thickness on the hemiplegic side was lower than that on the non-hemiplegic side (Supplementary material 2).