Ultrasonographic measurement of diaphragm thickness in patients with severe thoracic scoliosis

Abstract

Purpose

This study aimed to measure diaphragm thickness using ultrasound in adult patients with severe idiopathic scoliosis.

Methods

This prospective case–control study included patients with severe idiopathic scoliosis and a healthy control group. The control and patient groups’ demographic features, pulmonary function tests, diaphragm thickness, and thickening fraction measured using ultrasonography were compared.

Results

End-expirium values were similar between the two groups (p = 0.902). However, end of inspirium, change level, and diaphragm thickening fraction were significantly lower in the scoliosis group (p < 0.001 for all). Cobb degree values were inversely correlated with forced expiratory volume in 1 s (%) (r =  − 0.909, p < 0.001), forced vital capacity (%) (r =  − 0.887, p < 0.001), and end-inspirium thickness (r =  − 0.673 and p < 0.001) values. Furthermore, diaphragm thickness at the end of inspirium was positively correlated with forced expiratory volume in 1 s (%) (r = 0.636, p = 0.001) and forced vital capacity (%) (r = 0.646, p = 0.001) values. No significant correlation was found between diaphragm thickening fraction and forced expiratory volume in 1 s or forced vital capacity.

Conclusion

Ultrasound can provide valuable information about diaphragm morphology and quantify diaphragm contraction.

Introduction

Scoliosis is a common musculoskeletal disorder. It is the spinal deformity of the vertebrae characterized by a lateral curvature greater than 10 degrees and rotation [1, 2]. Scoliosis is either congenital, owing to vertebral malformations, or secondary to systemic and neuromuscular or idiopathic diseases, the latter being the most common [3]. Scoliosis can present with various symptoms such as shoulder, hip, or trunk asymmetry; trunk sliding; hump deformity; and psychosocial problems due to the aforementioned problems. Scoliosis can also cause pulmonary dysfunction due to spine and thorax deformities [4–6]. It has been well established that the convex or concave deformities in the thorax, formed by the rotation of the vertebrae in scoliosis patients, particularly in severe cases, can lead to pulmonary function disorders and restrictive lung disease by decreasing lung volume and thoracic wall compliance and displacing thoracic organs. Pulmonary function disorder has been associated with the severity of the Cobb angle, curvature location, curvature vertex, and concomitant thoracic hypokyphosis [7–9]. Here, the evaluation and proper management of pulmonary functions are mainly important in patients with scoliosis.

The diaphragm is the main respiratory muscle, and diaphragm contraction is associated with respiratory functions. In recent years, ultrasound (US) has gained increased utility to visualize the diaphragm and assess its function with several advantages [10–14]. The literature used different methods to examine the diaphragm in patients with scoliosis [15, 16]. However, US evaluation of the diaphragm in these patients has not been studied yet. Therefore, this study aimed to measure diaphragm thickness in adult patients with severe idiopathic scoliosis.

Methods

Study protocol and participants

The current study protocol was approved by the local ethics committee (no. 2019/576), and written informed consent was obtained from the participants. This study conforms to all Strengthening The Reporting Of Observational Studies İn Epidemiology (STROBE) guidelines and reports the required information accordingly (see Supplementary Checklist). This was a prospective case–control study conducted in a tertiary hospital. The patients were prospectively enrolled between January 2019 and January 2020; they all had main thoracic idiopathic scoliosis, required but neglected surgery, and had a Cobb angle of ≥ 45° measured in a coronal plane in a scoliosis graph with complete skeletal maturity [17, 18]. All patients had right thoracic curvature according to the apex of the scoliosis. The modified Cobb method was used to measure the severity of kyphosis in all patients [19]. Excluded from the study were patients with congenital spinal and costal anomalies, neuromuscular and neurological diseases, or respiratory system diseases affecting lung function; current smokers or those with previous history of smoking; patients younger than 18 years of age, and patients who cannot cooperate with spirometry. In addition, a group of healthy people without any known disease was formed as controls. The control group was selected from the hospital staff or patients’ relatives. The demographic features, pulmonary function tests (PFTs), and ultrasonography findings of the control group and the patient group were compared.

Ultrasonographic measurement

Ultrasonographic examinations were conducted by a single physician who was blinded to the patient groups. A US machine (Philips^® EPIQ 7, Philips Healthcare, Bothell, WA, USA) equipped with a high-resolution linear probe (Philips^® L18-5) was used for the examinations. With the patient in a supine position, the transducer was placed over the right chest wall (over the anterior axillary line) at the level of the ninth intercostal space (Fig. 1). After observing diaphragm movement during inspiration, the same physician performed the measurements at the end of maximum expiration and maximum inspiration. Diaphragm thickening fraction (DTf) (%) was calculated using the following formula: (thickness_{max insp} − thickness_{max exp})/thickness_{max exp} × 100.

Fig. 1.

Ultrasound measurement of the diaphragm. Through a high-resolution linear probe, the diaphragm is seen between two hyperechoic lines at the level of the ninth intercostal space and anterior axillary line. The superficial hyperechoic line refers to the pleura, and the deeper one corresponds to the peritoneum

Resting spirometry

PFTs were evaluated using conventional spirometric measurements (MasterScreen PFT, CareFusion, Hoechberg, Germany). Tests were conducted with the patients in a seated position and were repeated at least three times. Instructions were given, and maneuvers were shown for all cases before testing. Acceptable recordings were obtained from each maneuver, and the best values were considered. Spirometric parameters consisted of forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), and the ratio of FEV1 to FVC (FEV1/FVC) and were expressed as percentages of the normal predicted values.

Statistical analysis

Data were analyzed using the Statistical Package for the Social Sciences software. The Shapiro–Wilk test and histograms were used to confirm normality distribution. Descriptive data were expressed as mean ± standard deviation or number (n) and percentages (%). Student’s t-test (numeric variables) and Chi-square test (categorical variables) were employed for between-group comparisons. Pearson’s correlation coefficients were used for correlation analyses, with p < 0.05 considered statistically significant.

Power analysis was performed using GPower 9.1.2, and the sample size was determined as 14 participants for each group (total of 28). The effect size values were calculated by FEV1, FVC, end of inspirium, and thickening ratio measurements obtained from patients and controls in a pilot study. The minimum effect size (as 1.44 for FEV1) was selected to reach the maximum sample size. The allocation ratio was set at 1:1, the actual power was determined at 0.956, and type I error alpha was set at 5%. However, during the study period, 24 patients with scoliosis and 20 controls were enrolled.

Results

The scoliosis group consisted of 24 patients (9 males, 15 females) with a mean age of 33.5 ± 9.57 years (range 19–51 years) whereas the control group had 20 cases (6 males, 14 females) with a mean age of 30.85 ± 6.7 years (range 19–42 years). No significant differences were found between the groups in terms of age and body mass index. FEV1 (%) and FVC (%) values were significantly lower in the scoliosis group (p < 0.01 for all). For US measurements, the end-expirium values of the groups were similar (p = 0.902). However, end-inspirium, change level, and DTf values were significantly lower in the scoliosis group (p < 0.001 for all) (Table 1).

Table 1.

Comparison of the parameters between the groups

Variables	Scoliosis group	Control group	P value
Age (years)	33.50 ± 9.5	30.85 ± 6.7	0.305
Gender			0.601
Male	9 (37.5)	6 (30.0)
Female	15 (62.5)	14 (70.0)
Body mass index (kg/m2)	20.90 ± 1.8	21.58 ± 1.8	0.225
COBB	68.83 ± 23.0	N/A	N/A
FEV1 (%)	80.25 ± 10.3	91.59 ± 3.8	< 0.001
FVC (%)	91.37 ± 10.9	105.73 ± 4.5	< 0.001
FEV1/FVC	87.73 ± 1.9	86.67 ± 2.9	0.159
Diaphragm thickness
End-expirium (mm)	1.84 ± 0.1	1.84 ± 0.1	0.902
End-inspirium (mm)	3.12 ± 0.1	3.42 ± 0.1	< 0.001
Change level (mm)	1.28 ± 0.1	1.58 ± 0.1	< 0.001
Thickening ratio (%)	69.94 ± 3.4	86.24 ± 1.9	< 0.001

The data are given as mean ± standard deviation or n, (%)

Table 2 presents the correlation analyses. Cobb degree values were inversely correlated with FEV1 (%) (r =  − 0.909, p < 0.001), FVC (%) (r =  − 0.887, p < 0.001), and end-inspirium thickness (r =  − 0.673 and p < 0.001) values. Furthermore, diaphragm thickness at the end of inspirium was positively correlated with FEV1 (%) (r = 0.636, p = 0.001) and FVC (%) (r = 0.646, p = 0.001) values. No significant correlation was found between DTf and FEV1 or FVC (Table 2).

Table 2.

Correlation analyses

Variables		Cobb	Thickening fraction	End-expirium	End-inspirium	Change level	FEV1 (%)	FVC (%)	FEV1/FVC
Cobb	r	1	− ,206	− ,101	− ,673**	− ,363	− ,909**	− ,887**	− ,559**
	p		,334	,637	,000	,081	,000	,000	,004
Thickening fraction	r	− ,206	1	− ,897**	,329	,966**	,082	,083	,057
	p	,334		,000	,116	,000	,702	,700	,792
End-expirium	r	− ,101	− ,897**	1	,123	− ,752**	,215	,220	,066
	p	,637	,000		,568	,000	,312	,302	,760
End-inspirium	r	− ,673**	,329	,123	1	,563**	,636**	,646**	,264
	p	,000	,116	,568		,004	,001	,001	,213
Change level	r	− ,363	,966**	− ,752**	,563**	1	,243	,246	,121
	p	,081	,000	,000	,004		,252	,246	,574
FEV1 (%)	r	− ,909**	,082	,215	,636**	,243	1	,989**	,528**
	p	,000	,702	,312	,001	,252		,000	,008
FVC (%)	r	− ,887**	,083	,220	,646**	,246	,989**	1	,396
	p	,000	,700	,302	,001	,246	,000		,055
FEV1/FVC	r	− ,559**	,057	,066	,264	,121	,528**	,396	1
	p	,004	,792	,760	,213	,574	,008	,055

Bold p values denote significance

**Correlation is significant at the 0.01 level (2-tailed)

Discussion

This study aimed to measure diaphragm thickness using ultrasonography and evaluates its possible relationship with PFTs for the first time in the literature, to the best of our knowledge. This study had two main outcomes. First, DTf, diaphragm thickness at the end of maximum inspirium, FEV1, and FVC values were significantly lower in patients with scoliosis. Second, FEV1 and FVC were significantly correlated (positively) with diaphragm thickness at the end of inspirium. On the contrary, thickness at the end of inspirium was inversely correlated with the Cobb angle.

Decreased lung capacity, respiratory muscle function, and exercise capacity are common complications in patients with idiopathic scoliosis [3, 4, 6, 9, 20]. Many studies have found the relationship between PFTs and radiological parameters in scoliosis. However, previous studies used different imaging/assessment methods (magnetic resonance imaging, electrodiagnostic testing). In contrast to these studies, we used US to assess diaphragm thickness, which was the main strength of this study. Ultrasonography is widely and readily available, has high spatial resolution, and can provide dynamic imaging and a morphologic view of the diaphragm. In addition, US is patient friendly (noninvasive) and cheaper than other imaging methods [13, 21, 22]. According to our results, diaphragm thickness at the end of maximum expirium was similar in the groups. However, diaphragm thickness at the end of maximum inspirium and DTf significantly decreased in the scoliosis group. We believe that our results are noteworthy because DTf directly shows diaphragmatic contraction and is correlated with PFTs [23]. On the other hand, thickness at the end of inspirium was correlated inversely with Cobb angle values. As the Cobb angle increased, the end-inspirium thickness decreased.

Another main outcome that must be emphasized in this study is the lower FVC and FEV1 values in patients with scoliosis. Our findings were as expected because of the involvement of patients with severe scoliosis. In previous studies with different sample populations, FVC and FEV1 values were correlated with the change in DTf measured by US [23]. In our study, PFTs positively correlated with end-inspirium thickness; in other words, as the end-inspirium diaphragm thickness increased, better FEV1 and FVC values were obtained. Nonetheless, DTf and PFTs were not correlated.

Hence, we can say that US can “overall” provide information about diaphragm function and morphology. It can also be readily used as point-of-care or bedside evaluation in daily clinical practice to determine decreased respiratory functionality. Yet again, we emphasize that US measurement cannot replace PFTs. On the other hand, US can be helpful in the rehabilitation program of relevant patients. For instance, the use of real-time US imaging for diaphragm motion biofeedback is quite effective in improving the performance and retention of one’s diaphragm activation ability [24].

Since all patients analyzed in the current study had right curvature, the measurements were obtained from the right side. Patients with left curvature were excluded because the apex of the scoliosis curvature can change the outcomes. We tried to form a homogeneous group that mainly consisted of patients with right curvature. As mentioned in the literature, thoracic idiopathic scoliosis is commonly seen with right curvature, and left curvature can present with severe intraspinal, cardiopulmonary, or other anomalies [25]. However, one must note that the diaphragm is a large muscle with variable anatomy. Its different areas have varying structures of the muscle and tendineum. As such, different types of scoliosis can alter diaphragm structure.

Limitations

This study has some limitations. Electrodiagnostic methods are the gold standard in evaluating diaphragm function and contraction, but they are invasive and not easily applicable. In addition, user dependence on US examination and lack of diaphragm excursion are other limitations. Diaphragm excursion can vary depending on several technical parameters and is less accurate.

Conclusion

In light of our first and preliminary results, DTf, FEV1, and FVC values were lower in patients with scoliosis than in healthy subjects. Furthermore, FEV1 and FVC were correlated positively with end-inspirium diaphragm thickness, but end-inspirium thickness values were inversely correlated with Cobb angle values. In conclusion, US can provide valuable information about diaphragm morphology and quantify diaphragm contraction. The quantification of diaphragm contraction through US can “overall” guide physicians in identifying scoliosis patients with decreased pulmonary function but without skipping PFTs. However, considering the diagnostic accuracy and clinical use of US, further studies on this topic with larger sample sizes are definitely warranted.

Funding

This study received no funding.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.