Abstract
Objective
To evaluate the diagnosis performances of halo and compression signs alone and combined, assessed by a high frequency 22-MHz probe, and test their agreement in giant cell arteritis (GCA).
Methods
In this cross-sectional study on patients suspected with GCA, halo sign was defined as hypo or iso-echogenic circumferential aspect of the vessel wall in transverse or longitudinal view; and compression sign was defined as visibility of the vessel wall upon transducer-imposed compression of the artery. Agreement of the two signs was tested using the Cohen’s kappa statistic.
Results
A total of 80 patients (50% women) were included with a mean age of 74.4 years. Twenty participants (25%) were ultimately treated for GCA. Halo and compression signs have respective prevalences of 35% and 48%, with respective sensitivity and specificity of 80% and 80% for the halo sign; and 85% and 65% for the compression sign. The kappa coefficient for the global agreement of the two signs was 0.67 (95% confident interval: 0.54-0.85). Combination of the two signs give a sensitivity of 80% and a specificity of 81.7%.
Conclusion
Halo and compression signs assessed by a high frequency probe, show a good level of agreement for the diagnosis of GCA and improve ultrasound specificity when combined together.
Keywords: Giant cell arteritis, Ultrasound, High-frequency probe
Introduction
Giant cell arteritis is a systemic vasculitis affecting large and medium-sized arteries that can both be cranial and extra-cranial; among the cranial arteries, the most affected are the temporal arteries [1]. Patients with GCA present, in almost all cases, inflammation with increased levels of C reactive protein (CRP) and/or erythrocyte sedimentation rate (ESR) [2]. Patients with GCA are usually 50 years old or above and can have clinical manifestations including new-onset of, or new type of headache, temporal artery tenderness to palpation or decreased pulsation, jaw claudication, and visual disturbances (blindness or transient amaurosis); which should be considered as severity signs and should lead to the urgent initiation of corticosteroid therapy [3].
The diagnosis is based on a rigorous clinical approach, and confirmation always justifies a high-dose corticosteroid therapy. However, a strong clinical suspicion especially, if severity signs exist, requires the initiation of treatment as soon as possible before the completion of additional examination tools to confirm the diagnosis [4–7]. Among available imaging tools, Doppler ultrasound (DU) of the temporal arteries is recommended at the first line by the European League against Rheumatism (EULAR) since 2018; It allows the detection of halo sign, characterized by a hypoechoic (dark) thickening of the vessel wall, which has shown good diagnostic performances for GCA [8]. In 2013, a novel ultrasound sign was described by Aschwanden et al. as visibility of the temporal artery upon transducer-imposed compression of the artery and has shown an excellent inter-observer agreement [9, 10].
According to the 2018 EULAR recommendations, DU of temporal arteries for the diagnosis of GCA should be performed using probes with the B-mode frequency of at least 15 MHz; however, the compression sign was described using a linear 5–17 MHz broadband transducer [9]. With the development of new ultrasound technology, high frequencies probes are increasingly available and those with a frequency equal or greater to 20 MHz may allow better visualization of vessel walls of temporal arteries [11]. Very little data are available on the diagnosis performances of compression sign as well as halo sign assessed by high-frequency ultrasound transducer of more than 20 MHz. Moreover, since the description of the compression sign, whether it should be considered independently of the presence of the halo sign remains unclear, and if so, its agreement with the halo sign as well as the potential benefit of their combination for the diagnosis of GCA has been little described. We, therefore, conducted this study to clarify these questions.
Materials and methods
Study design and setting
This cross-sectional study was conducted from December 2019 to October 2020. Participants were recruited at the vascular medicine unit of the Brest university teaching hospital in France; they were seen once for data collection and DU realization. Data on their management by physicians in charge, and results of other paraclinical examinations were further collected from their medical files. All participants give oral consent, and a non-opposition form was established for all of them and the procedure of taking oral consent was approved by the France national personal protection committee (PPC EST I), which gave general approval for the study on the 4th of December 2019 on recorded number 29BRC190275. Administrative approvals were also obtained from authorities of the Brest university teaching hospital.
Participants
All patients suspected with GCA who were addressed to the vascular medicine unit of the Brest university teaching hospital, for DU of temporal arteries were approached for consideration to be enrolled in the study. Potentially eligible and consenting participants were consecutively included if they were aged 50 years old or above and had no history of GCA; this cutoff for age was decided based on the ACR (American College of Rheumatology) criteria for GCA. Clinical probability was accessed by the clinician addressing the patient (physicians in charge) based on clinical finding and ACR criteria [7].
Data collection
A standardized questionnaire was used for the data collection on age, gender, potential clinical signs of GCA, corticosteroid treatment if present, with duration since initiation and reason for initiation. We also collected the value of CRP and ESR when they were measured as well as results of temporal artery biopsy (TAB) and positron emission tomography (PET) of cranial arteries when they were performed. We finally recorded the result of DU carried out on all segments of the two temporal arteries of each participant.
Doppler ultrasound scanning technique
Bilateral DU evaluation of the temporal arteries was performed in all study participants using a « Toshiba Canon Aplio i800» (TOSHIBA, Tokyo, Japan, 2018) duplex ultrasound with a linear 22-MHz hockey stick probe (i22LH8). Scanning was conducted by four experienced operators, including three vascular medicine physicians and a vascular medicine trainee, all with good experience in the practice of temporal arteries’ DU (at least 100 exams each year for the less experienced of the team). The B-scan and Doppler settings were adjusted for the best assessment of the arteries. All the three segments of temporal arteries (common trunk, frontal and parietal branches) were scanned in the transverse and longitudinal sections. The gain and the dynamic range were set to allow the differentiation of the wall from the lumen of the vessel. The pulse repetition frequency (PRF) was set between 2 and 3.5 kHz depending on the flow velocity and the image depth which was set between 10 and 20 mm; the angle between sound waves and artery was always ≤ 60° as suggested by the 2018 EULAR recommendation’s [12]. Of note, DU examinations were not conducted blinded to clinical data but the operators only have access to the clinical signs presented by the patients (as they were reported on the prescription), and not to the diagnosis strategy of the physicians in charge of the patients nor to the results of others imaging examinations or TAB when performed. The ultrasound scanning technique used in our study has been described in detail and was recently published [13].
Definition of halo and compression signs
Halo sign was described as a hypoechoic circumferential dark aspect of the vessel wall in transverse or longitudinal view (Fig. 1) [14]. This sign shows the thickening of the vessel wall due to inflammation and some authors even considered it as a pathognomonic sign of GCA [15, 16], even if cases of false-positive halo exist, as it has been described in other diseases [17]. The compression sign was defined as visibility of the vessel wall upon transducer-imposed compression of the artery in the transverse section (Fig. 1); this sign has been described by Aschwanden et al. in 2013 and has shown good inter-observer agreement [9, 10]. Even if some authors consider these two signs as the same, with the hypoechoic aspect of vessel wall without compression sign being defined as a false positive halo sign (pseudo-halo), we decided to test them as two independents signs in our study. Aschwanden et al. even reported the fact that the compression sign was not tested independently from the halo sign in their study as a major limitation[9]. However, the final ultrasound diagnosis in our practice is based on the association of both signs.
Fig. 1.
A normal common right temporal artery (A); a common left temporal artery with halo sign (B), and a common right temporal artery with compression sign (C) in the same patient
Definition of the gold standard
The final diagnosis retained by the referring physician (rheumatologist and internal medicine specialist) of each participant was considered as the reference; with GCA patients being those finally diagnosed and treated with corticosteroid therapy for GCA by the referring physician. This information was retrospectively collected. In fact, TAB has been the gold standard test to diagnose GCA for many years, maybe because of its high specificity of 100%; but this test low sensitivity (54–76%), and can be misleading in a significant number of cases [18, 19]. In fact, up to 44% of patients with clinical features of GCA have negative histology; and there are many possible reasons for this, including the adequacy of the specimen, obtained, the duration of glucocorticoid treatment prior to biopsy, and the presence of skip lesions [19]. These limits and the development of other diagnosis tools in recent years have considerably challenged the place of TAB as the gold standard for the diagnosis of GCA. Moreover, the EULAR currently recommends using DU as the first diagnostic tool in the diagnosis strategy of GCA with as consequence in clinical practice, the fact that some patients are henceforth diagnosed and treat for GCA without TAB. We, therefore, decided to use the final diagnosis retained by the referring physician as the gold standard in our study as already done in the literature and reported in a systematic review by Duftner et al [20]. Three weeks After inclusion of the last patient in the study (8 months after inclusion of the first participant), we went back to the medical files of all participants to search if they finally received corticosteroid therapy for GCA or not, independently of the results of different exams they have undergone. Results of other imaging examinations done and/or TAB when performed were also collected at this time.
Statistical analysis
Data were analyzed using IBM Statistical Package for Social Sciences (SPSS) version 26.0. (IBM Corporation, New York, United States of America, 2019). Results are presented as frequency (percentage) for categorical variables and mean ± standard deviation (SD) for continuous variables. Groups’ comparisons were done using the Chi-square test, and the Student t-test or equivalents where appropriate. The agreement between the halo and compression sign was assessed using the Cohen’s Kappa statistic, presented with its 95% confidence interval (CI); its interpretation was done accordingly to the Landis and Koch classification (< 0: poor; 0–0.2: slight; 0.21–0.40: fair; 0.41–0.60: moderate; 0.61–0.80: substantial; 0.81–1: almost perfect) [21]. A p-value < 0.05 was used to characterize statistically significant results.
Results
General characteristics of the participants
Eighty patients agreed to participate in this study, of which 40 were women (50%). Their ages ranged from 50 to 93 years with a mean of 74.4 ± 10,6 years; with no difference between men and women (73.3 vs 75.5 years, p = 0.36). Except for the age of 50 years or older (present in all participant) and the abnormal TAB (not searched in all the patients), the most frequent ACR criteria were inflammation (defined as ESR ≥ 50 mm at 1st hour and/or CRP ≥ 6 mg/l), present in 56 participants (70%); unusual headaches present in 44 patients (55%); and the temporal artery clinical abnormality (temporal artery tenderness to palpation or decreased pulsation), present in 16 participants (20%). TAB was carried out in 11 participants, among which 3 had results consistent with GCA; 34 participants undergone PET, and 8 of them were compatibles with GCA. Of all participants, 13 (16%) were already on corticosteroid therapy at the time of the DU examination; the main reason for initiating this treatment was the presence of active polymyalgia rheumatica (54%). 4 patients (31%) were on corticosteroids for strong clinical suspicion of GCA; and were taking this treatment since a duration varying between 1 and 40 days (1, 4, 5, 40). A total of 160 temporal arteries were analyzed (two per patient) by DU. Of all participants, 20 (25%) were finally diagnosed and treated for GCA. General characteristics of the study population, as well as suspicious criteria for GCA and DU results, are summarized in Table 1 with a comparison of GCA and non-GCA patients.
Table 1.
Characteristics of the study population
| Overall (n = 80) | GCA + (n = 20) | GCA– (n = 60) | p | |
|---|---|---|---|---|
| General characteristics | ||||
| Mean age (years) ± standard deviation | 74.4 ± 10.6 | 73.5 ± 11.8 | 74.8 ± 10.3 | 0.9 |
| Gender (women), n (%) | 40 (50) | 9 (45) | 31 (52) | 0.61 |
| Corticosteroid therapy, n (%) | 13 (16) | 5 (25) | 8 (13) | 0.29 |
| Corticosteroid therapy for GCA suspicion, n (%) | 4 (31) | 3 (60) | 1 (12) | 0.31 |
| TAB done, n (%) | 11 (14) | 8 (40) | 3 (5) | < 0.001 |
| Positive TAB, n (%) | 3/11 (27) | 3/8 (38) | 0/3 (0) | 0.49 |
| PET done, n (%) | 34 (42) | 12 (62) | 22 (37) | 0.068 |
| Positive PET n (%) | 8/34 (24) | 8/12 (67) | 0/22 (0) | < 0.001 |
| Suspicious criteria for GCA | ||||
| Biological inflammation, n (%) | 56 (70) | 16 (80) | 40 (67) | 0.26 |
| New onset headache, n (%) | 44 (55) | 12 (60) | 32 (53) | 0.6 |
| Temporal arteries abnormalities, n (%) | 16 (20) | 5 (25) | 11 (18) | 0.53 |
| Unexplained fever, n (%) | 7 (8.8) | 2 (10) | 5 (8.3) | 0.99 |
| Doppler ultrasound finding | ||||
| Positive halo sign, n (%) | 28 (35) | 16 (80) | 12 (20) | < 0.001 |
| Positive halo sign left temporal arteries, n (%) | 25 (31) | 15 (75) | 10 (17) | < 0.001 |
| Positive halo sign right temporal arteries, n (%) | 24 (30) | 14 (70) | 10 (17) | < 0.001 |
| Bilateral halo sign, n (%) | 21 (26) | 13 (65) | 8 (13) | < 0.001 |
| Positive compression sign, n (%) | 38 (48) | 17 (85) | 21 (35) | < 0.001 |
| Positive compression sign left temporal arteries, n (%) | 34 (42) | 15 (75) | 19 (32) | < 0.001 |
| Positive compression sign right temporal arteries, n (%) | 34 (42) | 16 (80) | 18 (30) | < 0.001 |
| Bilateral compression sign, n (%) | 30 (38) | 14 (70) | 16 (27) | < 0.001 |
| n (%) Final ultrasound diagnosis (Halo and compression signs), n (%) | 27 (34) | 16 (80) | 11 (18) | < 0.001 |
GCA +: patients diagnosed with giant cell arteritis, GCA− patients considered free from giant cell arteritis, TAB temporal artery biopsy, PET positron emission tomography
Diagnosis performances of the halo sign
Among included patients, 28 (35%) had a halo sign. 25 participants (31%) had a halo sign on the left temporal artery, 24 (30%) had a halo sign on the right temporal artery and 21 (26%) had a bilateral halo sign (Table 2). In comparison with the gold standard, the halo sign had a sensitivity of 80%, a specificity of 80%, a positive predictive value of 57.1%, a negative predictive value of 92.3%, and an accuracy of 80% (p < 0.001) (Table 4). Note that the bilateral halo sign has a sensitivity of 65% and a specificity of 86.7%.
Table 2.
Halo sign in the study population
| Halo sign | |||
|---|---|---|---|
| Positive | Negative | Total | |
| Arterial segments | |||
| Left common trunk | 24 (30%) | 56 (70%) | 80 (100%) |
| Right common trunk | 21 (26%) | 59 (74%) | 80 (100%) |
| Left frontal branch | 15 (19%) | 65 (81%) | 80 (100%) |
| Right frontal branch | 17 (21%) | 63 (79%) | 80 (100%) |
| Left parietal branch | 13 (16%) | 67 (84%) | 80 (100%) |
| Right parietal branch | 16 (20%) | 64 (80%) | 80 (100%) |
| Temporal arteries | |||
| Left temporal artery | 25 (31%) | 55 (69%) | 80 (100%) |
| Right temporal artery | 24 (30%) | 56 (70%) | 80 (100%) |
| Bilateral | 21 (26%) | 59 (74%) | 80 (100%) |
| Patients | 28 (35%) | 52 (65%) | 80 (100%) |
Table 4.
Diagnosis performances of halo and compression signs
| Final GCA | |||
|---|---|---|---|
| No | Yes | Total | |
| Halo sign | |||
| Negative | 48 (80,0) | 4 (20,0) | 52 (65,0) |
| Positive | 12 (20,0) | 16 (80,0) | 28 (35,0) |
| Total | 60 (100,0) | 20 (100,0) | 80 (100,0) |
| Ss = 80,0% Sp = 80,0% PPV = 57,1% NPV = 92.3% Ac = 80% | |||
| Compression sign | |||
| Negative | 39 (65,0) | 3 (15,0) | 42 (52,5) |
| Positive | 21 (35,0) | 17 (85,0) | 38 (47,5) |
| Total | 60 (100,0) | 20 (100,0) | 80 (100,0) |
| Ss = 85,0% Sp = 65,0% PPV = 44,7% NPP = 92.9% Ac = 70.1% | |||
Ss sensitivity, Sp specificity, PPV positive predictive value, NPV negative predictive value, Ac accuracy
Diagnosis performances of compression sign
Of all participants, 38 (48%) had a compression; 34 (42%) had compression sign on the left temporal artery, 34 (42%) had a compression sign on the right temporal artery and 30 (38%) had a bilateral compression sign (Table 3). The compression sign compared to the gold standard, had a sensitivity of 85%, a specificity of 65%, a positive predictive value of 44.7%, a negative predictive value of 92.9%, and an accuracy of 70.1% (p < 0.001) (Table 3). Note that the bilateral compression sign has a sensitivity of 70% and a specificity of 73.3%.
Table 3.
Compression sign in the study population
| Compression sign | |||
|---|---|---|---|
| Positive | Negative | Total | |
| Arterials segments | |||
| Left common trunk | 30 (38%) | 50 (62%) | 80(100%) |
| Right common trunk | 31 (39%) | 49 (61%) | 80(100%) |
| Left frontal branch | 21 (26%) | 59 (74%) | 80 (100%) |
| Right frontal branch | 24 (30%) | 56 (70%) | 80 (100%) |
| Left parietal branch | 19 (24%) | 61 (76%) | 80 (100%) |
| Right parietal branch | 19 (24%) | 61 (76%) | 80 (100%) |
| Temporal arteries | |||
| Left temporal artery | 34 (42%) | 46 (57%) | 80 (100%) |
| Right temporal artery | 34 (42%) | 46 (57%) | 80 (100%) |
| Bilateral | 30 (38%) | 50 (62%) | 80 (100%) |
| Patients | 38 (48%) | 42 (52%) | 80 (100%) |
Agreement of halo and compression signs for the diagnosis of GCA
The halo and compression signs had a good level of agreement as attested by the substantial Kappa coefficient of 0.67 (95% confident interval: 0.54–0.85, p < 0,001). In fact, 27 participants (33.8) were considered to have GCA base on both halo and compression signs, while 41 (51.3%) were considered unaffected; which led to a percentage of agreement of 85.1% (Table 4). Considering analysis at arteries levels, the percentages of agreement between the halo and compression sign was 85.7% for a Kappa coefficient of 0.70 (95% confident interval: 95% CI 0.58–0.81, p < 0,001) (Table 5).
Table 5.
Agreement between halo and compression signs for GCA at patient’s level and at arteries’ level
Bold: percentages over all participants; Blue: agreement’ percentages
Among the 52 participants with negative halo sign, 11 had a positive compression sign but only 1 (9%) was finally considered as having GCA; while among the 42 participants with negative compression sign, 1 has a positive halo sign and was not finally diagnosed with GCA (data not shown). However, the combination of the two signs gave a sensitivity of 80%, a specificity of 81.7%, a positive predictive value of 59.3%, a negative predictive value of 92.5%, and an accuracy of 81.3% (p < 0.001) (Table 6).
Table 6.
Diagnosis performances of halo sign combined to compression sign
| Final GCA | |||
|---|---|---|---|
| No | Yes | Total | |
| Halo and compression sign (final ultrasound diagnosis) | |||
| Negative | 49 (81,7) | 4 (20,0) | 53 (66,3) |
| Positive | 11 (18,3) | 16 (80,0) | 27 (33,8) |
| Total | 60 (100,0) | 20 (100,0) | 80 (100,0) |
| Ss = 80,0% Sp = 81,7% PPV = 59,3% NPV = 92,5% Ac = 81.3% | |||
| Halo or compression sign | |||
| Negative | 38 (63,3) | 3 (15,0) | 41 (51,2) |
| Positive | 22 (36,7) | 17 (85,0) | 39 (48,8) |
| Total | 60 (100,0) | 20 (100,0) | 80 (100,0) |
| Ss = 85,0% Sp = 63,3% PPV = 43,6% NPV = 92,7% Ac = 68.8% | |||
Ss sensitivity, Sp specificity, PPV positive predictive value, NPV negative predictive value, Ac accuracy
Discussion
The mains findings from this study on the diagnosis performances and agreement between the halo sign and the compression sign in the diagnosis of GCA are the following: (1) prevalences of positive halo and compression signs were respectively 35% and 47.5%; (2) sensitivity and specificity were respectively 80% and 80% for the halo sign, and 85% and 65% for the compression sign; (3) despite the variations in sensitivity and specificity, halo and compression signs shown a good level of agreement for the diagnosis of GCA as attested by a substantial Cohen’s kappa coefficient of 0.67; and the combination of the tow signs improve the diagnosis performances of ultrasound for the diagnosis of GCA, as it leads to a sensitivity of 80%, and a specificity of 81.7%.
The prevalence of halo and compression sign in our study are similar to some previously described results with little variation [9, 18]. Even if these variations can be in part explained by the fact that DU is highly operator dependent, we strongly believe that the frequency of DU probes used may play a role. Indeed, EULAR recommendations suggest using DU probes with grayscale frequency of 15 MHz or above for examination of temporal arteries in diagnosis of GCA [22], but this was not the case for several published studies. Moreover, if DU was performed with a high-frequency transducer of more than 20 MHz (22 MHz) in our study, this was not the case in many previously published studies [23, 24].
The diagnosis performances of halo sign in our study were globally similar to previously described results and finding of some meta-analysis [25, 26]. However, considering the same gold standard used in our study, which was the final clinical diagnosis retained by the physician, the sensitivity and specificity of the halo sign reported in a meta-analysis by Duftner et al. were respectively of 77% and 96%, which are not too far from 80 and 80% found in our study. Nevertheless, we can realize that authors found a better specificity probably related to the variation of studies populations included in their review [20]. According to the diagnosis performances of compression sign, ours finding were similar to those of Aschwanden et al. in term of sensitivity (85% vs 79%); however, we found a very low specificity of 65% as compared to 100% described by the authors with a similar sample size [9]. These differences can be explained by the fact that our study population was a little older than the study population of the authors (mean ages: 74.4 vs 72 years); as the compression sign could be in some cases associated with atherosclerosis, which frequency increases with age [20]. Moreover, the gold standard was different in the two studies; the authors used ACR criteria while the final diagnosis retained by the physician was used in our study.
Based on the diagnosis performances reported in our study, we can be tempted to conclude that the compression sign is more sensitive than the halo sign and that the halo sign is more specific. However, considering the agreement of the two signs for the diagnosis of GCA, we found a good level of agreement as attested by the substantial Cohen’s kappa coefficient of 0.67 at the patient level and 0.70 at arteries level, corresponding to percentages of agreements of 85.1% and 85.7% respectively. Moreover, among patients considered without GCA based on halo sign, just one patient has a positive compression sign and was finally treated for GCA; conversely, among those considered without GCA by the compression sign, just one patient has a halo sign and was not finally tread for GCA; while the combination of the two signs gave a good sensitivity and specificity of 80% and 81.7% respectively. These results are in adequation with existing literature despite the fact that authors used a lower frequency transducer compared to the 22 MHz transducer used in our study [9].
Our study presents some limitations. First, we recruited our patients from only one site, this can be a source of bias and may hamper the generalization of our findings to the entire GCA suspected population. Second, our limited sample size, even if similar to some previously published studies, may decrease the power of our study. Third, the limited number of TAB in our sample did not allow us to evaluate ACR criteria for all participants, but it is clear that the place of TAB as the reference test in the diagnosis of GCA is henceforth challenged. Finally, the fact that the gold standard was the final diagnosis retained by the referring physician (not blinded to paraclinical data) and the fact that DU examinations were not conducted blinded to all clinical data, could reduce the quality of our study; nevertheless, the main aim of our study was to compare halo and compression signs assessed by a high-frequency ultrasound probe; instead of only giving the diagnosis performances of these tests, even if our findings are similar to existing data.
Our Study doesn’t only have limitations; its main strengths are represented by the fact that this is a one of the first studies to assess the GCA ultrasonographic sign (compression sign) using high-frequency transducer of more than 20 MHz, and one of the first study to assess the agreement of halo and compression signs based on well-known and recognized Kappa statistic as well as diagnosis performances of the two signs combined together.
Conclusions
Halo and compression signs assessed by high-frequency ultrasound probe, had good diagnosis performances for GCA, and a good level of agreement; moreover, the combination of these two signs give better sensitivity and good specificity than each sign alone. These findings attested to the good diagnosis performances of compression sign, assessed by high-frequency ultrasound probe, and confirm that the combination of this sign to halo sign improve the diagnosis performances of high-resolution doppler ultrasound in GCA. However, further studies on larger samples are needed to confirm these results.
Abbreviations
- ACR
American College of Rheumatology
- DU
Doppler ultrasound
- EULAR
European League against Rheumatism
- GCA
Giant cell arteritis
- MRI
Magnetic resonance imaging
- PET
Positron-emission tomography
- TAB
Temporal artery biopsy
Declarations
Funding
This research did not receive any specific funding.
Competing interests
The authors declare that they have no competing interests.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Ethics approval and consent to participate
Our study was conducted according to the ethical principles of medical research as stated in the declaration of Helsinki [27]. All participants give oral consent, and a non-opposition form was established for all of them and the procedure of taking oral consent was approved by the France National personal protection committee (PPC EST I), which gave approval for the study on the 4th of December 2019 on recorded number 29BRC190275.
Consent for publication
Not applicable.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.