Post COVID-19 Condition Patients with Dyspnea Show Diaphragm Dysfunction in Sonographic Imaging – a Prospective Observational Study

Abstract

Objective

Around 6.2% of patients report symptoms as fatigue, muscle pain and dyspnea more than three months after SARS-CoV-2 infection, defined as post COVID-19 condition (PCC). Non-hospitalized patients with PCC often show normal pulmonary functioning tests and imaging but suffer from respiratory symptoms. On clinical examination, PCC with dyspnea show signs of diaphragmatic dysfunction. The study aimed to objectively visualize and quantify the diaphragmatic function using sonographic parameters in PCC patients with and without dyspnea.

Materials and Methods

Adult PCC patients were prospectively assessed for dysfunctional breathing and diaphragmatic stiffness using sonographic imaging. Multiparametric sonography evaluated diaphragm thickness, mobility, stiffness and elasticity in different breathing cycles using B-mode imaging, M-mode and quantitative shear wave elastography. PCC patients were stratified into two groups with and without dyspnea.

Results

Fifty-four post-COVID patients were assessed, of whom n=24 (44.4%) reported dyspnea and presented dysfunctional breathing, while 30 PCC without dyspnea served as control. PCC with dyspnea compared to PCC without dyspnea showed a less deep first breath (5.8 mm vs. 6.5 mm, p=0.044), reduced diaphragm thickness on inspiration (3.4 mm vs. 3.9 mm, p=0.030), as well as less increase of diaphragmatic elasticity (108% vs. 146%; p=0.027) and diaphragmatic stiffness (40% vs. 53%; p=0.022) during inspiration.

Conclusions

Diaphragm dysfunction as a possible origin of dyspnea in PCC can be assessed and objectively quantified using multiparametric sonography and may help evaluate therapeutic interventions that are otherwise overlooked.

Zusammenfassung

Hintergrund und Ziel

Etwa 6,2% der Patienten berichten mehr als drei Monate nach einer SARS-CoV-2-Infektion über Symptome wie Müdigkeit, Muskelschmerzen und Atemnot, die als Post-COVID-19-Zustand (PCC) definiert werden. Nichthospitalisierte Patienten mit PCC weisen häufig normale Lungenfunktionstests und bildgebende Verfahren auf, leiden aber unter Atemwegssymptomen. Bei der klinischen Untersuchung zeigen PCC mit Dyspnoe Anzeichen einer Zwerchfelldysfunktion. Ziel der Studie war es, die Zwerchfellfunktion bei PCC-Patienten mit und ohne Dyspnoe anhand sonografischer Parameter objektiv darzustellen und zu quantifizieren.

Material und Methoden

Erwachsene PCC-Patienten wurden prospektiv auf dysfunktionale Atmung untersucht. Sonografisch wurden Zwerchfelldicke, -beweglichkeit, -steifigkeit und -elastizität in verschiedenen Atemzyklen mittels B-Mode, M-Mode und Scherwellenelastografie untersucht. Die PCC-Patienten wurden in zwei Gruppen mit und ohne Dyspnoe eingeteilt.

Ergebnisse

54 PCC-Patienten wurden untersucht, von denen 24 (44,4%) Dyspnoe und dysfunktionale Atmung aufwiesen, während 30 PCC-Patienten ohne Dyspnoe als Kontrolle dienten. PCC-Patienten mit Dyspnoe zeigten im Vergleich zurKontrollgruppe einen weniger tiefen ersten Atemzug (5,8 mm vs. 6,5 mm, p=0,044), eine geringere Zwerchfelldicke in Inspiration (3,4 mm vs. 3,9 mm, p=0,030) sowie eine geringere Zunahme der Elastizität (108% vs. 146%; p=0,027) und Steifigkeit (40% vs. 53%; p=0,022) in Inspiration.

Schlussfolgerungen

Eine Zwerchfelldysfunktion als mögliche Ursache der Dyspnoe bei PCC kann sonografisch beurteilt und quantifiziert werden und dazu beitragen weitere therapeutische Interventionen zu evaluieren.

Keywords

diaphragm dysfunction - post COVID-19 condition - dyspnea - functional disturbance - ultrasound

Schlüsselwörter

Diaphragma - Funktionelle Störung - Post-COVID Syndrom - Dyspnoe - Ultraschall

Introduction

The profound physical phenomenon of breathing that humans undergo each day, characterized by approximately 23,000 respiratory cycles that symbolize lifeʼs unyielding cadence. At the core of it lies the diaphragm, a pivotal musculature whose continuous and unabated contractions and relaxations regulate the flux of respiration.

Diaphragmatic sonography is an established examination used to assess atrophy, paralysis and diaphragm dysfunction [1] [2]. Sonographic examination of diaphragmatic thickness increase is already routinely performed at intensive care units, where it is considered a relevant parameter for successful weaning [3]. Furthermore, it is performed on COVID-19 patients, who have been hospitalized and intubated to evaluate successful extubation and assess diaphragmatic pathologies, such as diaphragmatic paresis [4]. M-mode technique can be employed to objectively measure the depth of breath, while elastographic examinations add a fast and non-invasive tool for assessment of tissue stiffness. During inspiration the stiffness of the diaphragm increases compared to expiration [4]. Furthermore, sonography of the diaphragm is mentioned to complement spirometry without relevant correlation to pulmonary function tests [5].

One concerning aspect in the aftermath of the COVID-19 pandemic is the prevalence of post-COVID-19 condition (PCC), which is around 6.2% [6]. The WHO defines PCC as persistent symptoms more than three months after the initial SARS-CoV-2 infection [7]. PCC can include a variety of symptoms, predominantly the persistence of respiratory problems. PCC affects both hospitalized and non-hospitalized patients, with women being more frequently affected than men. Respiratory issues following COVID-19 disease include a range of difficulties, such as shortness of breath, dyspnea, cough, or chest tightness. Chen et al. subsumed respiratory problems under the cluster dyspnea and found that dyspnea persists over time after COVID-19 infection [8].

The causes of respiratory problems after COVID-19 disease are complex and include the direct damage of the SARS-CoV-2 virus to lung tissue, as well as the bodyʼs immune response during the infection and functional impairments due to dysfunctional breathing [9] [10]. While lung function limitations and chronic pulmonary changes on chest imaging are common in patients with PCC who were hospitalized, these pathologies are rare in non-hospitalized patients [10].

Consequently, in the absence of abnormal findings in standard pulmonary function tests and radiology imaging, it arises the question if diaphragm dysfunction is a relevant aspect to be further examined.

The manual medical examination technique of the diaphragm is difficult to quantify objectively because it is based on subjective clinical examination and experience. Thus, we aimed to assess sonographic parameters of diaphragm function in post COVID-19 condition comparing patients with and without dyspnea.

Methods

Study design

This study was part of a monocentric prospective open-label observational study addressing symptom-based physiotherapy interventions for PCC. Recruitment took place from 02/01/2022 to 05/01/2023. We report of a subgroup which additionally received sonographic imaging regarding diaphragmatic function. The study included patients over 18 years of age with a history of at least one SARS-CoV-2 infection at least 12 weeks ahead and reporting persistent symptoms according to the WHO definition of PCC. Patients with dyspnea and functional diaphragmatic restrictions in the clinical examination, such as heightened rigidity or restricted range of motion [11], were enrolled into the “dyspnea group” (dPCC). As shown in [Table 1], patients with no respiratory symptoms (fatigue and/or muscle pain only) served as “non-dyspnea” control (nPCC).

Table 1 Demographics.

Metric	Post COVID-19 dyspnea	Mean±SD Median (IQR)	Post COVID-19 non-dyspnea	Mean±SD Median (IQR)	Group difference	p-value	Test
Group size (n)	24	30
F:M	15 : 9	19 : 11	0.95	Chi-square
Age	41.7±12 38.5 (12.8)	39.4±13 37.5 (19.5)	0.51	t-test
Height (cm)	171±9 173 (11.6)	174±9 172 (11.9)	0.23	t-test
Weight (kg)	74.1±15 72.3 (14.9)	74.8±14 75.3 (16.7)	0.85	t-test
BMI (kg/m2)	25.2±4 24.1 (4.5)	24.6±4 23.4 (5.1)	0.58	t-test

Note: Demographics are described by group. The continuous data are presented as means±SD and below in each line as median and (IQR).

F=female, M=male, BMI: body mass index.

Patients were excluded in case of pregnancy, known pathology of the diaphragm or superficial tissue, i. e. surgery or scars in the examination area, acute respiratory infection or structural respiratory disease of any other cause (e. g. pneumonia, consolidation, atelectasis) or hepatosplenomegaly ([Fig. 1]). Sonography was performed to investigate structural or functional differences of the diaphragm between both groups.

Fig. 1 Flow diagram of participant selection.

Sonographic imaging

Diaphragmatic sonography was performed using a high-end ultrasound system (Aplio i900, Canon, Otawara, Japan). All patients were examined in the supine position with head section angled at 30 degrees.

For dynamic assessment of the diaphragm (B-mode and M-mode imaging), a multi-frequency convex transducer with a penetration depth of 20 cm was used. Diaphragm thickness and shear wave elastography (SWE) parameters (e. g. elasticity and stiffness) were measured using a multifrequency linear transducer with a standardized penetration depth of 4 cm. For detailed description of the parameters see [Table 2].

Table 2 Examination protocol.

No.	Step	Description
1	Positioning of the patient	Supine position, head section tilted upwards by 30° degrees
	Screening both hemidiaphragms	Positioning a convex transducer lateral on both sides of the rib cage in the 8th to 10th intercostal space in the anterior to the midaxillary line to screen for unilateral pathology as hemiparesis or pleural effusion
2	Movement of the right hemidiaphragm	Convex transducer placed on the ventrolateral protion of the right rib cage in the 8th to 10th intercostal space near the anterior axillary line to use the liver as a transducer window; M-Mode to evaluate the excursion of the diaphragm in different breathing maneuvers
2.1	Breathing at rest	3 separate breathing cycles while breathinging at rest
2.2	Sniff test	3 separate breathing cycles during the sniff test
2.3	Deep breathing	3 separate breathing cycles during maximal inspiration and expiration
3	Conctraction of the right hemidiaphragm	Linear transducer placed on the ventrolateral protion of the right rib cage in the 8th to 10th intercostal space in the anterior and middle axillary line to assess the thickness of the diaphragm at the end of expiration and deep inspiration
3.1	Thickness at the end of expiration	Assessing the thickness of the diaphragm at the end of expiration in 3 separate breathing cycles
3.2	Thickness at the end of inspiration	Assessing the thickness of the diaphragm at the end of inspiration in 3 separate breathing cycles
4	Stiffness and elasticity of the right hemidiaphragm	Linear transducer placed on the ventrolateral protion of the right rib cage in the 8th to 10th intercostal space in the anterior and middle axillary line to assess the elasticity and stiffness of the diaphragm at the end of expiration and deep inspiration; To obtain accurate elastography measurements, it was deemed essential to establish the propagation and area of homogeneous shear waves as a prerequisite
4.1	Stiffness and elasticity at the end of expiration	Assessing the stiffness and elasticity at the end of expiration in 3 separate breathing cycles
4.2	Stiffness and elasticity at the end of inspiration	Assessing the stiffness and elasticity at the end of inspiration in 3 separate breathing cycles

Note: The following two sonography transducers with standardized settings were used. Convex transducer (i8xC1; MHz 5, Gain 80, dynamic range (DR) 70, penetration depth 20cm); linear transducer (iX18; MHz 18,2; Gain 80, dynamic range (DR) 70 and penetration depth of 4 cm).

Based on published protocols and recommendations [1] [2] the diaphragm was examined using the procedure shown in [Fig. 2]. [Table 2] provides a succinct overview of each assessment step. According to the EXODUS guidelines, experts agreed on unilateral measurement of the diaphragm as an acceptable proxy for the whole diaphragm if there is no suspicion of unilateral pathology [1].

Fig. 2 Representative figure of the examination protocol as described in [Table 2.] 1. Positioning of the patient and screening of both hemidiaphragms. 2. Movement of the right hemidiaphragm: Breathing at rest, sniff test, deep breathing. 3. Thickness of the right hemidiaphragm at the end of expiration and at the end of inspiration. 4. Stiffness / Elasticity of the right hemidiaphragm at the end of expiration and at the end of inspiration.

Following these methodological guidelines, we first evaluated the movement of the diaphragm on both sides by visual inspection with a convex transducer to avoid indications of possible unilateral pathologies. Afterward, all the following measurements (diaphragm excursion, thickness, and elasticity/stiffness) were performed unilaterally on the right side. Examination of the diaphragm was performed with a convex transducer placed on the ventro-lateral portion of the rib cage to use the liver as a transducer window. Therefore, different breathing maneuvers (rest, sniff, and deep breathing) were recorded in three separate breathing cycles each. In the M-Mode ultrasound tracing of the diaphragm, we measured the right hemidiaphragm excursion on the vertical axis, spanning from the baseline to the maximum height of inspiration on the graph ([Fig. 2]).

Subsequently, the diaphragm thickness was then measured at the end of expiration and inspiration in three separate breathing cycles. The transducer was placed in the 8–10th intercostal space between the anterior and middle axillary line. For inspiration, the quality standard was defined as displaying the lung shadow in the left portion of the screen (see [Fig. 2] section: 3 and 4). This ensures that the muscles studied also tense appropriately.

Shear wave elastography

Same image acquisition was performed as for thickness ([Table 2]). We assessed the stiffness and elasticity at the end of expiration and inspiration in three separate breathing cycles (overall 3 measurements for each condition).

To achieve accurate elastography measurements, it is imperative to establish the propagation and area of homogeneous shear waves as a prerequisite. The elastographic measurement in the region of shear wave propagation was selected by zooming in the simultaneously opened B-scan using a rectangle region of interest to solely measure the elasticity of the diaphragm.

Ethical considerations

The study was conducted in accordance with the Declaration of Helsinki in its currently applicable version. Ethical approval for the study was obtained from the local institutional review board (ethics committee) of*blinded*. All participants provided written informed consent. The study was registered in the National Clinical Trials Register*blinded*. The reporting complied with STROBE guidelines.

Data management and statistical analysis

The diaphragmatic thickening percentage (TFdi) was calculated as follows.

Furthermore, we investigated parameters based on SWE, the diaphragmatic elasticity index (dEI), as well as the diaphragmatic stiffening index (dSI), which were calculated similarly to the TFdi. All measurements were assessed at the end of inspiration and exspiration.

The indexes are calculated as follows:

Mean value of three consecutive replicates was calculated for each parameter per patient. Descriptive analyses included calculating group means and standard deviations (SD) for each parameter. In addition, median and interquartile range (IQR) are presented in [Table 1] [3] for each parameter. The t-test, or chi-square test were employed for comparisons between groups for demographic and clinical characteristics, as indicated. We performed intrapersonal comparisons of parameters using the paired t-test (see [Table 3]). The significance level was set at p<0.05, but trends (p<0.10) were reported as well. The statistical analyses were performed with R version 4.3.0.

Table 3 Group differences for sonographic parameters

Metric	Post COVID-19 dyspnea	Mean±SD Median (IQR)	Post COVID-19 non-dyspnea	Mean±SD Median (IQR)	Group difference	p-value
Diaphragm excursion breathing at rest (mm)	24.2±8.6 23.4 (14.3)	24.0±7.6 22.8 (13.4)	0.926
Diaphragm excursion sniff test (mm)	29.3±10.5 27.5 (12.2)	30.2±11.3 27.7 (10.1)	0.765
Diaphragm excursion deep breathing (mm)	59.2±11.6 62.7 (16.9)	64.8±10.3 65.2 (14.1)	0.072
Diaphragm thickness exsp (mm)	1.4±0.3 1.4 (0.4)	1.5±0.3 1.4 (0.4)	0.561
Diaphragm thickness insp (mm)	3.4±0.9 3.2 (1.1)	3.9±0.8 3.8 (1.1)	0.030
TFdi (%)	140.4±64.2 134.1 (57.0)	170.1±69.9 160.4 (59.9)	0.111
Diaphragm stiffness exsp (m/s)	2.2±0.4 2.1 (0.4)	2.0±0.3 2.0 (0.3)	0.134
Diaphragm elasticity exsp (kPa)	13.7±5.1 12.4 (4.8)	11.9±3.2 11.7 (3.8)	0.135
Depth of measurement SWE exsp (cm)	1.8±0.4 1.7 (0.6)	1.6±0.4 1.6 (0.6)	0.218
Diaphragm stiffness insp (m/s)	3.0±0.4 3.0 (0.4)	3.1±0.3 3.1 (0.6)	0.356
Diaphragm elasticity insp (kPa)	26.7±8.0 26.5 (6.8)	28.3±6.25 28.1 (10.4)	0.427
Depth of measurement SWE insp (cm)	1.8±0.5 1.7 (0.5)	1.6±0.3 1.6 (0.4)	0.237
Diaphragmatic elasticity index (%)	107.7±61.6 111.3 (87.3)	146.5±62.6 127.9 (82.3)	0.027
Diaphragmatic stiffening index (%)	40.5±20.9 42.6 (28.8)	53.2±17.9 48.1 (24.5)	0.022

Note: Demographics are described by group. The continuous data are presented as means±SD and below in each line as median and (IQR), expiration: exsp, inspiration: insp, diaphragmatic thickening percentage: Tfdi, shear wave elastography: SWE. Metric data were analyzed with t-test for group comparison. Significant p-values are marked in bold.

Results

Overall, n=54 post-COVID patients were enrolled in the study and fulfilled the inclusion criteria. On average, the patients were 40 years of age (SD: 12.4), their body mass index was 24.9 (SD: 3.89), and the gender distribution was 37% male to 63% female.

In total n=24 (44%) reported respiratory problems due to their post COVID-19 infection and showed a diaphragm dysfunction on manual medical examination (see [Table 1]) and thus were assigned to the dPCC group. 30 patients were assigned to the control group nPCC.

The two groups were comparable in age, sex, weight, height, and BMI ([Table 1]).

None of the patients reported chronic obstructive pulmonary disease (COPD). Three dPCC patients and two nPCC patients reported history of asthma, while being clinically unremarkable during study participation. Screening for unilateral malfunctions showed no indicator of hemidiaphragm paralysis or presence of pleural effusion on both sides of the diaphragm in each group.

The amplitude of diaphragmatic excursion during breathing at rest and in the sniff test for individual breaths and mean values showed similar results ([Table 3]).

For deep breathing, the diaphragmatic excursion was approximately 7 mm lower in dPCC group for the first breath measured, with a mean depth of 5.8 cm compared to 6.5 cm (p=0.044). This significant effect gradually decreased between the groups to 6 mm (p=0.070) and 4 mm (p=0.192) within the second and third breathing cycle.

Diaphragmatic thickness at the time of end-expiration was similar in both groups at 1.43 cm and 1.49 cm. While there was a general increase in diaphragmatic thickness in both groups during inspiration, compared to the expiratory breathing position, the diaphragmatic thickness in deep inspiration was significantly lower in dPCC patients (p=0.030). Accordingly, the TFdi was lower in dPCC patients (140.4% vs. 170.1%; p=0.11). Elasticity and stiffness increased within the same patient in both groups during inspiration compared to expiration (p<0.001 and p<0.001, [Table 2]). Of note, depth of SWE measurement was similar in both groups in expiration and inspiration (dPCC: 1.8 cm [SD: 0.4] vs. 1.8 cm [SD: 0.5]; nPCC: 1.6 cm [SD: 0.4] vs. 1.6 cm [SD: 0.3]).

Elasticity significantly increased in inspiration in both groups (dPCC: 13.75 kPa [SD: 5.05] vs. 26.73 kPa [SD: 7.99]; nPCC: 11.95 kPa [SD: 3.17] vs. 28.31 kPa [SD: 6.26]). Stiffness in the expiration of dPCC increased from 2.15 m/s (SD: 0.35) to 2.98 m/s (SD: 0.40), and in nPCC from 2.02 m/s (SD: 0.26) to 3.073 (SD: 0.33).

Diaphragm elasticity (p=0.135) and stiffness (p=0.134) in expiration were lower in the group without dyspnea than in the group with dyspnea. The opposite was observed for inspiration, in which the elasticity and stiffness were lower.

The diaphragmatic elasticity index (dEI) (108% vs. 146%; p=0.027) and the diaphragmatic stiffness index (dSI) (40% vs. 53%; p=0.022) showed a smaller increase in dPCC compared to nPCC patients. Main parameters are presented in [Fig. 3].

Fig. 3 Box plots for main parameters. Note: Patients with dyspnea referred as dPCC, patients without dyspnea referred as nPCC.

Discussion

The primary aim of this study was to evaluate if diaphragm dysfunction seen in clinical manual examination of PCC patients can be objectively visualized with multiparametric sonography (B-Mode imaging, M-Mode, and SWE).

The present study findings in 54 PCC patients in a single centre prospective trial indicate diaphragm dysfunction in dPCC patients.

The dPCC group demonstrated:

• less excursion of the diaphragm while deep breathing

• less thickness of the diaphragm in inspiration

• less increase in elasticity and stiffness of the diaphragm measured through shear wave elastography

Our results regarding diaphragm excursion and thickness align with the previously published norm values on diaphragmatic sonography recently summarized by Boussuges et al. 2020 [2]. The respiratory excursion in resting breathing and voluntary sniffing is comparable. The nPCC showed comparable depth on deep breathing and diaphragmatic thickness. Notably, the values for dPCC are in the lower range or outside the normative range.

Apart from the intensive care setting, point of care sonography is rarely used to assess diaphragm dysfunction. Noteworthy, impairment of the inspiratory muscle function has been described previously [12] and sonography may be helpful to evaluate diaphragm function. So far only a few studies are published concerning diaphragm mobility and thickness after a COVID-19 infection [13] [14] [15] [16] [17]. These studies mainly focused on patients recovering from severe COVID-19 infection with acute respiratory distress syndrome [13] [15] [16] [17].

Boussuges 2022 and Farr 2021 reported a smaller thickening fraction and less diaphragm motion while deep breathing [13] [16]. Both defined diaphragm dysfunction by a reduced thickening fraction and Boussuges proposed a classification of mild and severe hemidiaphragm dysfunction based on thickening fraction and reduced diaphragm excursion below the lower limit of normal [2]. By this classification none of the included dPCC in this study would have a diaphragm dysfunction. Eman et al. reported similar excursions for deep breathing and quiet breathing as Boussuges et al. [13] [15]. In this study post-COVID patients with dyspnea showed higher means of thickening fraction and a larger excursion while deep breathing. Reasons for the difference are highly likely due to disease severity. In our study only one dPCC patient had been hospitalized in the acute infection phase.

In addition, both reported severe dysfunctions like hemidiaphragm paralysis in two cases [13] and an elevated hemidiaphragm [16], which was an exclusion criteria in our study.

Only three of the five studies examined PCC patients according to the WHO definition [13] [14] [17]. None of the studies above examined diaphragm elasticity and stiffness based on SWE values.

Our results are in line with values derived from previously published studies regarding stiffness and elasticity at end of expiration and inspiration [18] [19] [20] [21]. We showed that dPCC patients have a tendency towards higher stiffness and elasticity values at the end of expiration and had a lower increase in inspiration. Interestingly, COPD patients showed a higher muscle stiffness at functional residual capacity compared to healthy controls [19]. Zhang et al. [22] reported that elasticity of the diaphragm at functional residual capacity increases with disease progression and exacerbations in COPD. While Flattres et al. [23] described means for expiratory elasticity that are comparable to post-COVID patients with dyspnea in our study. In line to other studies [18] [20], we found lower levels for elasticity and stiffness in expiration. The present literature pertaining to the elastography of the diaphragm is limited. However, as previously proposed [20], it holds potential for further investigation as it may aid in evaluating diaphragm dysfunction based on SWE. While the diaphragmatic thickening percentage is widely used and an important marker for weaning success on intensive care unit [3], we endorse calculation of the dEI and dSI for diaphragm dysfunction because stiffness is used as a surrogate parameter for contraction of muscle fibres. Strengthening this thesis, Arrab and colleagues found that a reduction of stiffening was associated with muscle weakness and injury in critically ill patients [21]. Based on our results we hypothesize that the reduced thickeness and stiffness of the diaphragm can be considered as a sign of diaphragm dysfunction. This impairment of the inspiratory muscle strength in mildly to moderate affected dPCC patients has only been evaluated with spiroergometric measurement so far [12]. Coinciding with this hypothesis, a higher diaphragm thickness in inspiration showed to correlate with muscle strength [24].

The advantage of our study is that, unlike earlier studies in PCC, we assessed the different aspects of the diaphragm with sonographic imaging including its movement, thickness, elasticity, and stiffness in a one-stop examination. Multiparametric sonography of the diaphragm seems to provide an opportunity to objectively visualize and better comprehend a PCC symptom that might otherwise be challenging to categorize. This imaging approach is patient-centered as a quantitative value for a somatic origin of the symptom dyspnea, affirming that it is more than a psychological nature.

Limitations

Our study included a relatively small sample size, which may have resulted in underpowering and potentially leading to unidentified relationships between variables. In addition, it was conducted mono-centrically at a single university center, which may lead to selection bias.

A standardized pulmonary functioning wasn’t performed right before diaphragm sonography to compare dysfunctional breathing. However, in cases with uncertainties due to medical history prior to study inclusion data, we obtained information prior to inclusion of the study. Standardized radiological imaging like X-ray or CT was only performed in unexplained or persistent symptoms as recommended.

Of note, diaphragm sonography needs another approximately 15 minutes, with fluctuations primarily due to the SWE measurement during inspiration. The challenge lies in the fact that the lung that is viewed from the left side extends towards the measurement area of elastography. On the other hand, it is a one-stop examination and the first modality to help clarify the symptom dyspnea.

Conclusion

Our research found significant differences in dynamic B-Mode imaging and stiffness/elastography between dyspneic and non-dyspneic PCC patients, indicating the potential for multiparametric sonography in PCC diagnostics and treatment. Given that we breathe approximately 23,000 times a day, disturbed diaphragm function might contribute to symptoms like fatigue and physical restrictions. Thus, early integration of functional imaging can be helpful for diagnostics and therapeutic evaluation, contributing to the restitution or rehabilitation process in post-COVID-19 condition.

Conflict of Interest

The authors declare that they have no conflict of interest.

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Publication History

Received: 04 October 2024

Accepted after revision: 07 January 2025

Article published online:
06 February 2025