
==== Front
J Chest Surg
J Chest Surg
Journal of Chest Surgery
2765-1606
2765-1614
The Korean Society for Thoracic and Cardiovascular Surgery

38600812
10.5090/jcs.23.134
jcs-57-5-430
Clinical Research
Routine 6-Week Outpatient Radiography and Visit in Patients with Conservatively Treated Multiple Rib Fractures: Valuable or a Waste of Resources?
https://orcid.org/0009-0006-5654-5028
Peuker Felix B.Sc. 123
https://orcid.org/0009-0000-5864-7454
Bosch Thomas Philip B.Sc. 24
https://orcid.org/0000-0003-3497-659X
Houwert Roderick Marijn M.D., Ph.D. 1
https://orcid.org/0000-0003-2298-244X
Hoepelman Ruben Joost M.D. 1
https://orcid.org/0000-0002-0886-1847
Niemeyer Menco Johannes Sophius M.D. 1
https://orcid.org/0000-0003-4209-1193
van Baal Mark M.D., Ph.D. 1
https://orcid.org/0000-0003-3595-7307
Minervini Fabrizio M.D., Ph.D. 5
https://orcid.org/0000-0002-7277-3438
Beeres Frank Johannes Paulus M.D., Ph.D. 23
https://orcid.org/0000-0003-1882-8626
van de Wall Bryan Joost Marinus M.D., Ph.D., M.Sc. 23
1 Department of Trauma Surgery, University Medical Center Utrecht, Utrecht, The Netherlands
2 Department of Orthopedic and Trauma Surgery, Cantonal Hospital Lucerne, Lucerne, Switzerland
3 Department of Health Sciences and Medicine, University of Lucerne, Lucerne, Switzerland
4 Department of Trauma Surgery, Leiden University Medical Center, Leiden, The Netherlands
5 Department of Thoracic Surgery, Cantonal Hospital Lucerne, Lucerne, Switzerland
Corresponding author Felix Peuker Tel 31-647597078 Fax 31-088-75-555-04 E-mail felix@peuker.nl ORCID https://orcid.org/0009-0006-5654-5028
5 9 2024
11 4 2024
11 4 2024
57 5 430439
25 9 2023
26 1 2024
5 2 2024
Copyright © 2024, The Korean Society for Thoracic and Cardiovascular Surgery
2024
https://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background

This study investigated the incidence and clinical consequences of abnormal radiological and clinical findings during routinely performed 6-week outpatient visits in patients treated conservatively for multiple (3 or more) rib fractures.

Methods

A retrospective analysis was conducted among patients with multiple rib fractures treated conservatively between 2018 and 2021 (Opvent database). The primary outcome was the incidence of abnormalities on chest X-ray (CXR) and their clinical consequences, which were categorized as requiring intervention or additional clinical/radiological examination. The secondary focus was the incidence of deviation from standard treatment in response to the findings (clinical or radiological) at the routine 6-week outpatient visit.

Results

In total, 364 patients were included, of whom 246 had a 6-week visit with CXR. The median age was 57 years (interquartile range, 46–70 years) and the median Injury Severity Score was 17 (interquartile range, 13–22). Forty-six abnormalities (18.7%) were found on CXR. These abnormalities resulted in additional outpatient visits in 4 patients (1.5%) and in chest drain insertion in 2 (0.8%). Only 2 patients (0.8%) with an abnormality on CXR presented without symptoms. None of the 118 patients who had visits without CXR experienced problems.

Conclusion

Routine 6-week outpatient visits for patients with conservatively treated multiple rib fractures infrequently revealed abnormalities requiring treatment modifications. It may be questioned whether the 6-week outpatient visit is even necessary. Instead, a more targeted approach could be adopted, providing follow-up to high-risk or high-demand patients only, or offering guidance on recognizing warning signs and providing aftercare through a smartphone application.

Multiple rib fractures
Conservative treatment
Follow-up
Radiography
Funding This work was financially supported by DePuy Synthes; grant number DPS-TCMF-2017-036 and registered in the Netherlands Trial Register (NTR6833).
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pmcIntroduction

Rib fractures are a common occurrence in blunt thoracic trauma [1]. The standard treatment for multiple (3 or more) rib fractures, excluding flail chest, is conservative management, which consists of adequate analgesics, pulmonary physiotherapy, and respiratory support if needed [2]. Once patients are discharged, many hospitals in the Netherlands and Switzerland routinely plan an outpatient visit with a chest X-ray (CXR) after 6 weeks [3]. This time point is based on the standard intervals advised by the Arbeitsgemeinschaft für Osteosynthesefragen for all fractures. The clinical and radiological examinations performed during this visit are typically aimed at detecting potential complications and assessing pain levels [4].

There is increasing evidence challenging the value of routine outpatient clinic visits and follow-up X-rays after traumatic fractures. A recent example is a randomized trial comparing routine 6-week X-rays to a reduced imaging approach in patients treated operatively for ankle fractures. This study showed no benefit of routine X-rays with regard to complications, functional outcomes, and pain [5]. This adds to existing evidence regarding the environmental impact of healthcare. In the Netherlands, a substantial 22% of all CO2 emissions from the healthcare sector are attributed to the travel movements of healthcare staff and patients [6].

To the best of our knowledge, no studies have specifically investigated the value of CXR performed at the 6-week outpatient visit in patients with conservatively treated (multiple) rib fractures. Furthermore, the overall clinical value of this visit—both clinical and radiological—has not been examined. With healthcare burdens and costs on the rise, it is important to re-evaluate established clinical pathways, such as the routine 6-week visit and CXR, in order to determine whether they are still truly necessary in modern times.

The primary objective of this study was to determine the incidence of abnormalities observed on CXRs at the routine 6-week outpatient visit and evaluate their clinical consequences in patients treated conservatively for multiple rib fractures. The secondary outcome of interest was the incidence of deviation from normal management protocols in response to findings (clinical and/or radiological) at the routine 6-week outpatient visit.

Methods

Study design

This study is a retrospective analysis of all patients treated conservatively for multiple rib (non-flail) fractures included in the Opvent database in 2 out of the 6 level-1 trauma centers. The Opvent study is an international observational multicenter prospective study that included all patients with multiple rib fractures (treated both surgically and conservatively) between 2018 and 2021 [3]. In the Opvent study, patients with clinical flail chest or thorax deformity were treated operatively. Patients where a numerical rating scale score <5 could not be achieved with oral, intravenous and/or epidural analgesic treatment were also treated operatively. For patients without clear indications for surgery, treatment allocation (conservative or operative) was determined by the geographical location of the trauma and natural variation in preferred treatment methods among hospitals and countries [2,3,7]. Three centers treated these patients conservatively and 3 centers operatively. Thus, only 2 out of 6 trauma centers were selected for this study, as they were found to have included the majority of conservatively treated patients (598/873). The patients included in the present study were aged 18 years or older, were diagnosed with 3 or more computed tomography (CT)-confirmed rib fractures after blunt trauma, treated conservatively, and had an outpatient visit at 6 weeks after trauma. The exclusion criteria were surgical treatment and clinical flail chest. All patients, including those who did not visit the hospital at 6 weeks, were contacted by phone to ascertain whether their course of disease was uneventful 1 year after trauma. Patients were considered lost to follow-up when they had no physical 6-week check-up for any reason. Patients without a physical check-up were contacted by telephone to determine the reason for their absence.

This study adhered to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [8]. Institutional review board approval of the University Medical Center Utrecht was obtained (NTR6833). Informed consent was obtained from all individual participants included in the study.

Baseline characteristics

The following patient and trauma characteristics were collected: sex, age, and American Society of Anesthesiologists score. The injury-related characteristics were the Injury Severity Score (ISS), the number of rib fractures, and the incidence of polytrauma and concomitant injuries (e.g., pneumothorax, hemothorax, pulmonary contusion, and sternum and clavicle fractures) [9-11]. Polytrauma was defined as an ISS≥16 and isolated thoracic injury as an Abbreviated Injury Scale score >2 for the thorax ≤2 for the other regions [12].

The following in-hospital parameters were collected: length of hospital stay, length of intensive care stay, incidence of invasive mechanical ventilation, insertion of chest drainage, and complications (i.e., pneumonia, pleural effusion, hemothorax, and pneumothorax). Pleural effusion, hemothorax and pneumothorax were classified as complications in case of any increase after the initial imaging post-trauma, independent of any treatment that was initiated. Pneumonia was defined as an infection of the lower respiratory tract with clinical signs and symptoms (temperature >38.5°C, auscultation suspected of infiltrate, purulent sputum, leukocytosis, and elevated C-reactive protein levels) requiring antimicrobial treatment [13].

Outcomes

The primary outcome of interest was the incidence of abnormalities seen on 2-plane CXR 6 weeks after trauma (e.g., rib dislocation, pleural effusion, or pneumothorax). An abnormality was defined as any new finding on the 6-week CXR compared to the last CXR taken before discharge. CXRs were administered as part of routine care at 6 weeks after trauma; however, all CXRs between 4 and 8 weeks after trauma were considered eligible. All abnormalities were categorized according to their clinical consequences, which included “no consequence,” “additional examination” (clinical and/or radiological) or “intervention.”

The secondary outcome of interest was the incidence of deviation from normal treatment protocols in response to findings (clinical and/or radiological) at the routine 6-week outpatient visit. As it was normal policy to discharge patients from outpatient follow-up after 6 weeks, all additional visits, interventions, or radiological examinations were considered a deviation. All outcomes are described separately for patients with isolated thoracic injuries and patients with combined injuries (thoracic injuries and concomitant injuries in other regions).

Statistical analysis

Statistical analyses were performed using IBM SPSS ver. 26.0 (IBM Corp., Armonk, NY, USA). All categorical variables are presented as counts with percentages (%). Continuous variables are presented as means and standard deviation for parametric data, or as median with interquartile range for nonparametric distributed data. The Shapiro- Wilk test was performed and Q-Q plots were drawn to evaluate the distribution of continuous variables. Nonparametrically distributed variables were compared using the Mann-Whitney U test (for ordinal/continuous variables) and the Pearson chi-square test (for dichotomous variables).

Results

In total, 598 patients managed conservatively for multiple rib fractures were identified from the database between January 2018 and March 2021. Of these, 233 patients were excluded (49 flail chest patients and 80 patients with surgically treated rib fractures). Of the 469 eligible patients, 104 were lost to follow-up; thus, 364 patients were included in the final analysis, of whom 246 (67.6%) had an outpatient visit with CXR and 118 patients (32.4%) had a visit without CXR. Fig. 1 shows a flowchart of patient inclusion.

Analysis of missing cases

Patients who were lost to follow-up had a higher intensive care unit (ICU) admission rate (35.6% versus 20.1%, p<0.001) and more frequently acquired in-hospital pneumonia (20.2% versus 11.0%, p=0.014) or developed in-hospital pneumothorax (6.7% versus 1.1%, p=0.003). All other baseline characteristics were comparable (Table 1).

Baseline characteristics

The baseline characteristics of all included patients are described in Table 1, and the baseline in-hospital parameters are presented in Table 2. Patients attending a 6-week outpatient visit without CXR had more concomitant sternum fractures than patients attending a check-up with CXR (12.2% versus 5.1%, p=0.033).

Primary outcome

A total of 46 abnormalities (18.7%) were found in the 246 patients who had a 6-week CXR. All abnormalities and their clinical consequence are described in Table 3. These abnormalities only had clinical consequences in 6 patients (2.4%), including an additional outpatient visit (n=4) and chest drainage (n=2). These patients are listed in Appendix 1. Thirty-one of the 46 abnormalities occurred in patients with isolated thoracic injuries, while 15 were observed in patients with combined injuries.

Of the 4 patients (case numbers 2, 3, 5, and 6) who required an additional visit, 3 experienced symptoms (difficulty swallowing, dyspnea, and rib shifting; case numbers 2, 3, and 6, respectively) (Appendix 1). The other patient had asymptomatic pneumothorax (case number 5), which resolved spontaneously during follow-up and did not require any intervention.

Of the 2 patients who received a chest drain, 1 experienced light dyspnea and 1 was asymptomatic. A detailed description of the clinical course of these patients can be found in Appendix 1 (case numbers 1 and 4).

Secondary outcomes

When focusing on the 6-week outpatient visit as a whole (both clinical and radiological findings), there were 2 patients with normal CXR findings who still experienced severe pain, prompting an additional outpatient visit to be scheduled (case numbers 7 and 8). These patients add up to the 7 previously described patients whose management changed based solely on their CXR. Eventually, 1 patient (case number 8) was treated for non-union of rib fractures. A detailed description of all patients whose treatment changed can be found in Appendix 1.

None of the 118 patients who had a 6-week visit without CXR experienced any problems. These patients were all discharged from outpatient follow-up.

Discussion

Summary of results

This study included 364 patients, of whom 246 had a follow-up visit with CXR and 118 patients had a follow-up visit without CXR. In 46 patients, an abnormality was found on CXR. These abnormalities had clinical consequences in only 6 patients, of whom 2 received chest drainage for pleural effusion and 4 had an additional visit planned. Notably, 4 of these 6 patients had symptoms indicating an abnormal course of disease. Additionally, there were 2 patients with severe pain and a normal CXR, who eventually were diagnosed with non-union of rib fractures based on a CT scan.

Comparison to previous literature

To our knowledge, only 2 studies have been published thus far that provide information on the value of follow-up CXR following rib fractures. In a retrospective study conducted by Deluca et al. [14] in 2022, a low incidence rate of pneumothorax/hemopneumothorax requiring tube thoracostomy (1.6%, n=6) was observed at 1-week CXR in patients with fewer than 3 traumatic rib fractures. Sixty-five percent of the patients presented with respiratory distress, indicating the presence of a complication. Other symptoms were not mentioned. Based on their findings, the authors concluded that scheduled follow-up CXR examinations appear to be unnecessary. Instead, they recommended “symptom-triggered reappearance” for follow-up evaluations.

Bansidhar et al. [15] in 2002 also performed a comparable retrospective study. Among the 58 participants, only 2 individuals experienced a change in management as a direct consequence of the CXR. Regrettably, the authors neither provided the time interval between trauma and follow-up CXR, nor reported on whether the 2 patients were symptomatic or asymptomatic. They concluded that it is not necessary to perform routine follow-up CXR unless there is evident clinical deterioration.

It should be acknowledged that the aforementioned studies did not focus on CXR 6 weeks after trauma in patients with multiple rib fractures, as described in the present study. Nonetheless, if the likelihood of finding an abnormality 1 week after trauma on CXR is already small, the chances of finding an abnormality at 6 weeks should logically be even smaller.

Interpretation of results and clinical implications

It should be noted that changes in the treatment policy based on clinical and/or radiological findings during the 6-week outpatient visit were rare. If they did occur, the majority of patients (5 out of 7) demonstrated symptoms indicating an abnormal course of disease. Additionally, pleural effusion and small pneumothoraxes were frequently found 6 weeks after trauma. These, however, have little clinical implications when patients are asymptomatic, as they tend to resolve spontaneously [16]. The minor significance of radiological findings was also pointed out in a prospective study by Sweet et al. [17] on CXR after chest tube removal in patients with multiple rib fractures; 31% (n=68) of post-removal CXRs showed intrathoracic pathologies, but only 3% (n=2) needed re-intervention. These findings prompt the question of whether the 6-week outpatient visit and routine CXR are necessary or could be omitted.

Omitting the 6-week visit, however, would inevitably lead to missing asymptomatic patients who have a complication requiring treatment that is only detectable by CXR. Although the risk is extremely small, one should ask oneself how much one is willing to accept at the benefit of decreasing the healthcare burden and costs. Moreover, a follow- up visit also contributes to a certain level of reassurance for both the patient and the surgeon. It should also be taken into account that rib fractures are frequently accompanied by other injuries. Therefore, a follow-up appointment frequently encompasses the evaluation of not only rib fractures, but also other injuries (e.g., clavicle, sternum, scapula fractures). The decision to skip or arrange a follow-up visit, with or without CXR, should be thoughtfully considered.

There are several alternatives that might solve these problems, while simultaneously limiting the number of 6-week visits. For instance, the treating surgeon may be more selective in planning follow-up visits and only offer these visits to patients who strongly prefer them or in situations where careful monitoring is warranted due to specific reasons (e.g., comorbidities, necessary follow-up for other injuries, or difficulties during initial treatment). Secondly, physical visits could be replaced by telephone check-ups if a physical check-up is not indicated per se. Thirdly, mobile e-health applications could also be used as a replacement for routine follow-up visits during the initial weeks after treatment. These applications could assess daily questionnaires alerting patients when a visit should be planned, while providing them with instructions on aftercare [18,19]. Several applications are already in use in other fields (e.g., for the conservative treatment of non-complicated fractures) that have proven their worth by reducing the number of outpatient clinic visits by 91% and follow-up imaging by 72% [20].

Limitations

There are several limitations that need to be considered. Firstly, there was a considerable number of patients who were lost to follow-up (104/364). Missing case analysis showed differences in baseline characteristics, with a higher need for ICU admission and a higher incidence of pneumonia and pneumothorax among the missing patients compared to the included cases. This might be a sign suggesting some degree of selection bias. These patients apparently had a more severe initial course of disease and would also be expected to have a higher chance of developing complications during follow-up, which should contribute to a higher incidence of abnormalities on CXR or clinical examination at the 6-week visit. However, we could not think of a logical explanation for why a treating physician would structurally refrain from following up with patients more strictly if the initial course was already abnormal. It might very well be possible that these differences were caused by mere chance. Additionally, the occurrence of complications such as pneumonia and/or pneumothorax are both related to the need for ICU admission. As such, it is not unexpected to find that multiple variables differ from the included cases if there is a correlation between them.

Secondly, it is essential to recognize the retrospective nature of this study and the exclusion of operated patients from the analyses and outcomes. Surgically treated patients most likely had more severe injuries and potentially were more prone to develop adverse events during follow-up. Therefore, the results in the present study, which are based on a conservatively managed group, cannot be extrapolated to surgically managed patients.

Thirdly, this study was conducted at 2 level-1 trauma centers. The results cannot be directly extrapolated to level-2 and level-3 centers, where the proportion of polytrauma patients would be lower. Nevertheless, as monotrauma patients have a lower likelihood of developing complications, the proportion of patients with abnormal findings during the 6-week follow-up visit would logically be even lower.

Conclusions

The routine 6-week outpatient visit, with or without CXR, for patients with conservatively treated multiple rib fractures seldom reveals abnormalities requiring treatment modifications. In rare cases of complications, patients almost always demonstrate symptoms prompting the need for further evaluation. It may be questioned whether, in light of these findings, the 6-week outpatient visit is even necessary. Instead, a more targeted approach could be adopted.

Acknowledgments

This work was part of the activities of the Natural Experiments Study Group (www.next-studygroup.org).

Article information

Fig. 1 Flow chart of patients in the study. CXR, chest X-ray; TP, treatment protocol.

Table 1 Baseline patient and trauma characteristics

Characteristic	Total	Included patients	Missed cases	p-value	
	
Total	Check-up with CXR	Check-up without CXR	p-value	
Total	468	364	246 (67.6)	118 (32.4)		104		
Demographic data								
Age at trauma (yr)	57 (46–70)	57 (46–68)	58 (46–70)	55 (42–66)	0.235	57 (47–72)	0.687	
Male sex	327 (69.9)	256 (70.3)	170 (69.1)	86 (72.9)	0.460	71 (68.3)	0.686	
ASA score								
1–2	352 (75.2)	281 (77.2)	183 (74.4)	98 (83.1)	0.065	71 (68.3)	0.063	
3–4	116 (24.8)	83 (22.8)	63 (25.6)	20 (16.9)	0.065	33 (31.7)	0.063	
Smokera)	89 (19.0)	71 (19.5)	46 (18.7)	25 (21.2)	0.585	18 (17.3)	0.673	
Injury-related characteristics								
ISS	17 (13–22)	17 (13–22)	16 (13–22)	17 (14–22)	0.440	16 (13–22)	0.404	
Polytrauma (ISS=16)a)	245 (52.4)	193 (53.0)	123 (50.0)	70 (59.3)	0.095	52 (50.0)	0.586	
No. of rib fractures	5 (4–7)	6 (4–7)	6 (4–8)	6 (4–7)	0.143	5 (4–6)	0.140	
Isolated thoracic injury	282 (60.3)	215 (59.1)	146 (59.3)	69 (58.5)	0.874	67 (64.4)	0.321	
Abbreviated Injury Scale								
Head	1 (0–2)	1 (0–2)	1 (0–2)	1 (0–2)	0.435	1 (0–2)	0.819	
Neck	0 (0–0)	0 (0–0)	0 (0–0)	0 (0–0)	0.364	0 (0–0)	0.973	
Spine	0 (0–2)	0 (0–2)	0 (0–2)	0 (0–2)	0.255	0 (0–2)	0.272	
Abdomen	0 (0–0)	0 (0–0)	0 (0–0)	0 (0–0)	0.766	0 (0–0)	0.062	
Concomitant injuries								
Pneumothorax	206 (44.0)	168 (46.2)	118 (48.0)	50 (42.4)	0.316	38 (36.5)	0.081	
Hemothorax	86 (18.4)	66 (18.1)	44 (17.9)	22 (18.6)	0.861	20 (19.2)	0.799	
Pulmonary contusion	170 (36.3)	140 (38.5)	101 (41.1)	39 (33.1)	0.142	30 (28.8)	0.072	
Sternum fracture	46 (9.8)	36 (9.9)	30 (12.2)	6 (5.1)	0.033	10 (9.6)	0.934	
Clavicle fracture	100 (21.4)	76 (20.9)	52 (21.1)	24 (20.3)	0.861	24 (23.1)	0.630	
Values are presented as number of patients (%) or median (interquartile range). Statistically significant results are marked in bold.

CXR, chest X-ray; ISS, Injury Severity Score.

a)Might not add up due to missing data.

Table 2 Baseline in-hospital parameters

Variable	Total	Included patients	Missed cases	p-value	
	
Total	Check-up with CXR	Check-up without CXR	p-value	
Total	468	364	246 (67.6)	118 (32.4)		104		
Hospital length of stay	8 (4–13)	8 (4–13)	8 (4–13)	6 (3–13)	0.168	8 (4–16)	0.717	
Need for ICU admission	110 (23.5)	73 (20.1)	46 (18.7)	27 (22.9)	0.351	37 (35.6)	<0.001	
ICU length of stay	2 (1–5)	3 (1–5)	2 (2–5)	3 (1–6)	0.884	2 (2–5)	0.977	
Need for IMV	67 (14.3)	49 (13.5)	33 (1.4)	16 (13.6)	0.970	18 (17.3)	0.323	
Need for chest drainage	126 (26.9)	100 (27.5)	72 (29.3)	28 (23.7)	0.470	26 (25.0)	0.154	
Complications								
Pneumonia	61 (13.0)	40 (11.0)	31 (12.6)	9 (7.6)	0.155	21 (20.2)	0.014	
Pneumothorax	11 (2.4)	4 (1.1)	1 (0.4)	3 (2.5)	0.508	7 (6.7)	0.003	
Hemothorax	13 (2.8)	9 (2.5)	7 (2.8)	2 (1.7)	0.067	4 (3.8)	0.452	
Empyema	0	0	0	0	NA	0	NA	
Pleural effusion	9 (1.9)	5 (1.4)	5 (2.0)	0	0.119	4 (3.8)	0.105	
Other complications	115 (24.6)	86 (23.6)	65 (26.4)	21 (17.8)	0.070	29 (27.9)	0.374	
Values are presented as number of patients (%) or median (interquartile range). Statistically significant results are marked in bold.

CXR, chest X-ray; ICU, intensive care unit; IMV, invasive mechanical ventilation; NA, not available.

Table 3 Number of abnormalities found on 6-week X-rays and their consequences

Variable	Pleural effusion	Pneumothorax	Secondary dislocation	Total	
Deviations from the standard protocol for patients with isolated thoracic injury (n=146)					
No clinical consequences	19 (13.0)	0	8 (5.5)	27 (18.5)	
Additional outpatient visit	1 (0.7)	1 (0.7)	1 (0.7)	3 (2.1)	
Chest drainage	1 (0.7)	0	0	1 (0.7)	
Deviations from the standard protocol for patients with combined injuries (n=100)					
No clinical consequences	9 (9.0)	2 (2.0)	2 (2.0)	13 (13.0)	
Additional outpatient visit	1 (1.0)	0	0	1 (1.0)	
Chest drainage	1 (1.0)	0	0	1 (1.0)	
Values are presented as number of patients (%).

Author contributions

Conceptualization: FP, RMH, RJH, MCPMB, FM, FJPB, BJMW. Data curation: FP, RJH. Formal analysis: FP, BJMW. Investigation: FP, TPB, MJSN. Methodology: FP, RMH, RJH, MCPMB, FM, FJPB, BJMW. Project administration: FP. Validation: FP. Visualization: FP, MJSN. Writing: FP, TPB, RMH, RJH, MJSN, MCPMB, FM, FJPB, BJMW. Resources: TPB. Supervision: RMH, RJH, MCPMB, FM, FJPB, BJMW. Final approval of the manuscript: all authors.

Conflict of interest

No potential conflict of interest relevant to this article was reported.
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