Abstract
Background:
ASBO is a frequent abdominal surgical emergency and a leading cause of morbidity and mortality in emergency surgery. The aim of this study is to provide insight into the current management of adhesive small bowel obstruction (ASBO) and associated outcomes.
Methods and materials:
A nationwide prospective cross-sectional cohort study was conducted. All patients with clinical signs of ASBO admitted to participating Dutch hospitals were included during a 6 months inclusion period between April 2019 and December 2020. Ninety-day clinical outcomes were described and compared for nonoperative management (NOM) and laparoscopic and open surgery.
Results:
In 34 participating hospitals, 510 patients were included, of whom 382 (74.9%) had a definitive diagnosis of ASBO. Initial management consisted of emergency surgery in 71 (18.6%) patients and NOM in 311 (81.4%) patients, 119 (31.1%) of whom required delayed surgery after failure of NOM. Surgical interventions started laparoscopically in 51.1%, of which 36.1% were converted to laparotomy. Intentional laparoscopy resulted in shorter hospital stays compared with open surgery (median 8.0 vs. 11.0 days; P<0.001) and comparable hospital mortality (5.2 vs. 4.3%; P=1.000). Oral water-soluble contrast use was associated with a decreased length of stay (P=0.0001). Hospital stay for surgical patients was shorter in patients who were operated on within 72 h of admission (P<0.001).
Conclusion:
This nationwide cross-sectional study demonstrates shorter hospital stay in ASBO patients who received water-soluble contrast, were operated within 72 h of admission or were operated with minimally invasive techniques. Results may support the standardization of ASBO treatment.
Keywords: adhesions, ASBO, small bowel obstruction
Introduction
Highlights
We conducted a nationwide prospective cross-sectional cohort study to provide insight into the current management of adhesive small bowel obstruction (ASBO) and associated outcomes.
Hospital stay was shorter in ASBO patients who received water-soluble contrast, was operated on within 72 h of admission or were operated with minimally invasive techniques.
Results may support the standardization of ASBO treatment.
Adhesive small bowel obstruction (ASBO) is a common complication of abdominal and pelvic surgery, causing significant morbidity and mortality1. Adhesions develop in 70–90% of patients undergoing open surgery, and in 45–60% of patients undergoing minimally invasive surgery2–4. Adhesions cause a lifetime risk of ASBO. Incidence of ASBO in the first years after surgery is estimated at 2–3% after any abdominal procedure and up to 10% after colorectal procedures1,5. Admission for ASBO results in significant morbidity and a 2.5% in-hospital mortality rate1. Following operative treatment, 30-day mortality is even estimated at 7%6. The risk of recurrence following an episode of ASBO is high, estimated at 15% after 3.5 years for patients operated for ASBO and 20% for patients who had successful nonoperative management (NOM)7.
In contrast to the burden of ASBO for patients, there is a paucity of studies evaluating various aspects related to the diagnosis and treatment of ASBO8,9. Many important aspects, such as the optimal timing of surgery after NOM, the role of water-soluble contrast (WSC) in the diagnosis and management of ASBO, and the role of minimally invasive operative techniques, are still not fully elucidated. In the past decade, the treatment of ASBO has slowly evolved. An initial trial of NOM, with gastric decompression, nil per os, and intravenous (i.v.) fluids, has become the standard of care10,11. With the progressive implementation of minimally invasive techniques and skills, laparoscopy is increasingly used for operative management of ASBO; however, clear selection criteria are lacking12–14. A caveat of minimally invasive techniques is the potential increase in the risk of iatrogenic injuries when patients are not adequately selected15. On the other hand, minimally invasive surgery for ASBO reduced time to recovery and might still be underused because skilled gastrointestinal surgeons and laparoscopy teams are not universally available for emergency service14.
The aim of this cross-sectional study was to assess current practice and related outcomes of the management of ASBO in the Netherlands, with emphasis on WSC use, minimally invasive techniques, and timing of surgery after failed NOM. With this explorative study of routine daily practice, we aimed to generate hypotheses for future research in order to improve the standards of care for ASBO.
Methods
We performed a national prospective cross-sectional cohort study using a collaborative snapshot research design, including all consecutive patients with a suspicion of ASBO during 6 months in each participating hospital between April 2019 and December 2020 (clinicaltrials.gov). The snapshot design is described in more detail in previous publications of the Dutch Snapshot Research group16. All Dutch hospitals were contacted to participate, and local collaborators completed web-based Case Report Forms, which were constructed in Castor (Castor EDC, 2019, the Netherlands), a certified clinical data management system. Data included symptomatology, diagnostic tests (laboratory tests and radiologic imaging), treatment strategies, ICU admission, hospital stay, mortality, complications, readmission, and recurrent ASBO. The medical ethical committee reviewed and approved this study (2018-4214). The work has been reported in line with the STROCSS (strengthening the reporting of cohort, cross-sectional and case–control studies in surgery) criteria, Supplemental Digital Content 1, http://links.lww.com/JS9/A547 17.
Patients
All adult patients who presented with a suspicion of ASBO (nausea with vomiting or absence of stools, abdominal distention, abdominal pain) were eligible. Exclusion criterium was a previously known other cause of small bowel obstruction (SBO), that is neoplasm or abdominal hernia. The follow-up period was 90 days. Written informed consent from all patients was obtained at admissions by a local research partner.
Subgroups and outcome measures
In patients with a definitive diagnosis of ASBO at discharge, diagnostic imaging studies and initial management were described. Comparisons were made between patients undergoing definitive NOM, emergency surgery (ES), and delayed surgery (DS) after the failure of NOM. Clinical outcome measures included length of stay, ICU admission rate, mortality, readmission, and recurrence. Subgroup analyses were performed for patients receiving WSC at admission, patients undergoing surgery after failure of NOM within 72 h and after a delay of more than 72 h, based on the Bologna guidelines10. In patients undergoing surgical treatment (emergent or after the failure of NOM), baseline characteristics and clinical outcomes were compared between intentional laparoscopic and primary open surgery. Conversion from laparoscopic to open surgery was categorized as strategic or due to intraoperative complications. The laparoscopic group was analyzed by the intention-to-treat principle (converted patients in the laparoscopy group) and by the definitive treatment received (converted patients in the open group). Previous operations of all patients were categorized by common groups of surgical procedures using the classification from the SCAR update studies (appendectomy, cholecystectomy, procedures on the colon, rectum, liver, or upper gastrointestinal tract, urological, gynecological procedures without uterus extirpation, gynecological procedures with uterus extirpation, retroperitoneal surgeries, or other)18. For subgroup analyses, patients who had more than one previous abdominal procedure were assigned to the category with the highest risk of readmissions related to adhesions in the SCAR update study so that each patient would only be included in one category18.
Furthermore, we assessed if a selection of laparoscopy was according to the Farinella criteria13. The Farinella criteria are a list of patient characteristics that can be used to select patients in whom laparoscopic treatment of ASBO is feasible and safe. The more points on the Farinella criteria, the less appealing laparoscopy for ASBO is. The criteria include less than two previous laparotomies, a single appendectomy or peritonitis, onset of symptoms less than 24 h before the presentation, the absence of peritonitis, ischemia or strangulation, and the experience of an operating surgeon.
Statistical analysis
All outcome measures were analyzed for the overall cohort and for predefined subgroups. Normally distributed continuous variables were presented as means with standard deviation. In the case of non-normal distribution, a median with minimum–maximum range was presented. Dichotomous or categorical data were presented as absolute numbers and percentages. We conducted an ANOVA (analysis of variance), Kruskal–Wallis test, independent t-test, Mann–Whitney U test, Chi-square (χ 2), Fisher–Freeman–Halton or Fisher’s exact test comparing data between groups as appropriate. All data were analyzed using the statistical program IBM Statistical Package for Social Sciences (SPSS, Chicago, Illinois, 2018) version 26.0 with a significance threshold of P<0.05.
Results
Study population
From 34 centers in the Netherlands, a total of 513 patients were included. Three patients were excluded due to incomplete data files. Symptoms at presentation were abdominal pain (n=413, 81.0%), nausea (n=392, 76.9%), vomiting (n=359, 70.4%), absence of stool (n=236, 46.3%), and abdominal distension (n=155, 30.4%). At discharge, 382 (74.9%) patients had a definitive diagnosis of ASBO (Fig. 1). All patients with a diagnosis other than ASBO at discharge were excluded from further analysis, and demographics and outcomes of these patients are presented in Supplementary Table 1 (Supplemental Digital Content 2, http://links.lww.com/JS9/A548) and Supplementary Table 2 (Supplemental Digital Content 2, http://links.lww.com/JS9/A548).
Figure 1.
Flowchart of inclusion of patients with the suspicion of adhesive small bowel obstruction (ASBO), initial and definitive treatment groups of patients with ASBO and operatively treated subgroups. NOM, nonoperative management.
Treatment strategy
NOM was started in 311 patients (81.4%); in 192 patients (61.7%), it was successful, whereas 119 patients underwent delayed surgery (38.3%) (Table 1). Emergency surgery was performed in 71 patients (18.6%). Patients were largely comparable at baseline for the three treatment strategies (definitive NOM, ES, or DS). Patients who underwent ES had a higher ASA (American Society of Anesthesiologists physical status classification) score compared with the other treatment strategies. Patients in the NOM group had a higher number of previous abdominal surgeries, more often underwent previous surgery on colon or rectum and had a higher number of ASBO episodes. Patients in the NOM group less frequently had a virgin abdomen (5.2%) compared with patients in the ES (23.9%) or DS (14.3%) group.
Table 1.
Demographics of the study population, data presented as n (%), mean (SD), and median [minimum–maximum].
| Diagnosis ASBO at discharge N=382 | ||||||
|---|---|---|---|---|---|---|
| Total, N=510 | ASBO, N=382 (74.9%) | Definitive NOM, N=192 (50.3%) | Emergency surgery, N=71 (18.6%) | Delayed surgery, N=119 (31.1%) | Sig. P | |
| Sex | 246 (48.2) male | 190 (49.7) male | 96 (50.0) male | 36 (50.7) male | 58 (48.7) male | 0.961 |
| Age (year) | 67.57 (15.3) | 67.18 (15.9) | 66.20 (16.3) | 68.35 (14.8) | 68.05 (15.9) | 0.479 |
| WHO performance index | 0.688 | |||||
| 0 | 155 (30.4) | 119 (31.2) | 56 (29.9) | 24 (33.8) | 39 (32.8) | |
| 1 | 192 (37.6) | 147 (38.5) | 79 (41.1) | 23 (32.4) | 45 (37.8) | |
| 2 | 116 (22.7) | 83 (21.7) | 38 (19.8) | 17 (23.9) | 28 (23.5) | |
| 3 | 38 (7.5) | 27 (7.1) | 16 (8.3) | 5 (7.0) | 6 (5.0) | |
| 4 | 3 (0.6) | 2 (0.5) | 0 | 1 (1.4) | 1 (8.0) | |
| ASA classification | 0.018 | |||||
| 1 | 54 (10.6) | 45 (11.8) | 26 (13.5) | 7 (9.9) | 12 (10.1) | |
| 2 | 267 (52.4) | 202 (52.9) | 106 (55.2) | 27 (38.0) | 69 (58.0) | |
| 3 | 164 (32.2) | 117 (30.6) | 52 (27.1) | 31 (43.7) | 34 (28.6) | |
| 4 | 20 (3.9) | 14 (3.7) | 4 (2.1) | 6 (8.5) | 4 (3.4) | |
| Charlson comorbidity index | 3.00 [0–13] | 3.00 [0–13] | 3.00 [0–13] | 3.00 [0–11] | 3.00 [0–9] | 0.419 |
| 0 | 146 (28.6) | 112 (29.3) | 59 (30.7) | 22 (31.0) | 31 (26.1) | 0.971 |
| 1 | 46 (9.0) | 34 (8.9) | 17 (8.9) | 5 (7.0) | 12 (10.1) | |
| 2 | 89 (17.5) | 70 (18.3) | 38 (19.8) | 12 (16.9) | 20 (16.8) | |
| 3 | 104 (20.4) | 79 (20.7) | 37 (19.3) | 15 (21.1) | 27 (22.7) | |
| ≥4 | 125 (24.5) | 87 (22.8) | 41 (21.4) | 17 (23.9) | 29 (24.4) | |
| Number of previous ASBO episodes | <0.001 | |||||
| 0 | 422 (82.7) | 311 (81.4) | 140 (72.9) | 65 (91.5) | 106 (89.1) | |
| 1 | 53 (10.4) | 43 (11.3) | 29 (15.1) | 4 (5.6) | 10 (8.4) | |
| 2 | 23 (4.5) | 17 (4.5) | 14 (7.3) | 1 (1.4) | 2 (1.7) | |
| ≥3 | 12 (2.4) | 11 (2.9) | 9 (4.7) | 1 (1/4) | 1 (0.8) | |
| ≥1 Operative management | 48 (9.4) | 40 (10.5) | 30 (15.6) | 3 (4.2) | 7 (5.9) | 0.004 |
| NOM only | 56 (11.0) | 46 (12.0) | 36 (18.8) | 3 (4.2) | 7 (5.9) | <0.001 |
| Number of previous operations | <0.001 | |||||
| 0 | 61 (12.0) | 44 (11.5) | 10 (5.2) | 17 (23.9) | 17 (14.3) | |
| 1 | 178 (34.9) | 133 (34.8) | 61 (31.8) | 27 (38.0) | 45 (37.8) | |
| 2 | 121 (23.7) | 91 (23.8) | 46 (24.0) | 11 (15.5) | 34 (38.6) | |
| ≥3 | 150 (29.4) | 114 (29.8) | 75 (39.1) | 16 (22.5) | 23 (19.3) | |
| ≥1 Laparotomy | 320 (62.7) | 247 (64.7) | 141 (73.4) | 36 (50.7) | 70 (58.8) | 0.001 |
| Laparoscopy only | 41 (8.0) | 28 (7.3) | 10 (5.2) | 7 (9.9) | 11 (9.2) | 0.276 |
| Type of previous surgery | 0.001 | |||||
| No abdominal surgery | 61 (12.0) | 44 (11.5) | 10 (5.2) | 17 (23.9) | 17 (14.3) | |
| Cholecystectomy | 11 (2.2) | 8 (2.1) | 4 (2.1) | 2 (2.8) | 2 (1.7) | |
| Gynecological with uterus extirpation | 27 (5.3) | 19 (5.0) | 7 (3.6) | 3 (4.2) | 9 (7.6) | |
| Gynecological no uterus extirpation | 20 (3.9) | 17 (4.5) | 6 (3.6) | 4 (5.6) | 7 (5.9) | |
| Liver | 0 | 0 | 0 | 0 | 0 | |
| Appendectomy | 47 (9.2) | 40 (10.5) | 16 (8.3) | 9 (12.7) | 15 (2.6) | |
| Urological | 21 (4.1) | 18 (4.7) | 9 (4.7) | 3 (4.2) | 6 (5.0) | |
| Upper gastrointestinal | 17 (3.3) | 11 (29) | 5 (2.6) | 4 (5.6) | 2 (1.7) | |
| Retroperitoneal | 0 | 0 | 0 | 0 | 0 | |
| Other | 118 (23.1) | 91 (23.8) | 50 (26.0) | 19 (26.8) | 22 (18.5) | |
| Colon | 139 (27.3) | 98 (25.7) | 60 (31.3) | 7 (9.9) | 31 (26.1) | |
| Rectum | 49 (9.6) | 36 (9.4) | 25 (13.0) | 3 (4.2) | 8 (6.7) | |
ASA, American Society of Anesthesiologists physical status classification; ASBO, adhesive small bowel obstruction; NOM, nonoperative management; SD, standard deviation; WHO, World Health Organization.
In-hospital mortality was 1.6% after NOM, compared with 5.6% after ES and 4.2% after DS, which was not significantly different (Table 2). Out of the three patients who died after undergoing definitive NOM, a complication that might have contributed to their mortality was identified. Specifically, one patient had urosepsis, while the other patient had pneumonia. Hospital stay was significantly shorter after NOM with a median of 3 days [0–36] compared with 7 [0–52] after ES and 11 [2–129] after DS. The rate of ICU admission, was also significantly lower after NOM (1.0%) compared with the two other groups (21.1% ES and 21.8% DS).
Table 2.
Outcomes study population and specific treatment groups, data represented as n (%), mean (SD), and median [minimum–maximum].
| Diagnosis ASBO at discharge, N=382 | ||||||
|---|---|---|---|---|---|---|
| Total, N=510 | ASBO, N=382 (74.9%) | Definitive NOM, N=192 (50.3%) | Emergency surgery, N=71 (18.6%) | Delayed surgery, N=119 (31.1%) | Sig. P | |
| LOS (day) | 5 (11.01) | 8.41 (11.19) | 3 [0–36] | 7 [0–52] | 11 [2–129] | <0.001 |
| In-hospital mortality | 16 (3.1) | 12 (3.1) | 3 (1.6) | 4 (5.6) | 5 (4.2) | 0.177 |
| ICU admission | 52 (10.2) | 43 (11.3) | 2 (1.0) | 15 (21.1) | 26 (21.8) | <0.001 |
| Duration (days) | 1.00 [1–35] | 1.00 [1–35] | 2.5 [1–4] | 2.00 [1–11] | 1.00 [1–35] | 0.540 |
| Readmission | 78 (15.3) | 56 (14.7) | 33 (17.2) | 11 (15.5) | 12 (10.1) | 0.256 |
| Recurrence | 54 (10.6) | 38 (9.9) | 30 (15.6) | 4 (5.6) | 4 (2.4) | <0.001 |
| Complications | 24 (4.7) | 18 (4.7) | 3 (1.6) | 7 (9.9) | 8 (6.7) | |
ASBO, adhesive small bowel obstruction; ICU, intensive care unit; LOS, length of stay; NOM, nonoperative management.
Overall, the number of readmissions at 90 days of follow-up was comparable between the three groups. However, in the NOM group, the number of readmissions for recurrence of ASBO was significantly higher compared with surgically treated patients (NOM 15.6%, ES 5.6%, DS 2.4%). In contrast, patients undergoing operative treatment had a higher number of readmissions for complications of treatment (NOM 1.6%, ES 9.9%, DS 6.7%). In all three groups, the most readmissions were in patients who had previous surgery on the colon (NOM 20.0%, ES 28.6%, DS 16.7%).
Imaging and water-soluble contrast use
In almost all patients, a computed tomography (CT) scan was performed during admission (n=330, 86.4%). The vast majority of all CT scans were made within 24 h of admission (n=300, 90.9%). Twenty patients initially had an abdominal ultrasound, followed by a CT scan in all 20 patients. All 71 patients who underwent ES had a CT scan prior to surgery.
Water-soluble contrast
Oral WSC was administered in 98 patients (25.7%) at the time of admission, with subsequent direct imaging in 86 patients, predominantly by CT scan (n=74). Five patients receiving WSC at admission had no imaging during their admissions, and all quickly recovered with NOM. Fifty patients who had WSC at admission had follow-up imaging, predominantly by X-ray (n=46). Contrast passage toward the colon was seen in 28 (60.9%) patients. One patient (3.6%) in whom contrast had passed to the colon within 24 h underwent surgery during admission compared with eight patients (44.4%) in whom contrast had not passed to the colon within 24 h (P<0.001).
Of all patients who were definitively treated using NOM (n=192), 70 (36.5%) received WSC immediately on admission, and 122 (63.5%) received no WSC on admission. Length of stay was significantly shorter in patients who received contrast during admission [LOS median 2.0 days (interquartile range – IQR 2–3.25) vs. 3.0 days (IQR 2–5); P=0.001].
Minimally invasive surgery
In Tables 3 and 4, an overview of demographics and outcomes in patients who underwent either ES or DS is provided, respectively categorized for intentional surgical approach and definitive surgical approach. In 97 patients (51.1%), adhesiolysis was performed by laparoscopic intent. In 35 patients (36.1%), conversion to open surgery was needed. The main reasons for conversion were a strategic conversion (n=10, 28.6%) and major bleeding (n=5, 14.3%).
Table 3.
Demographic features and outcomes in patients treated surgically for adhesive small bowel obstruction (ASBO), based on the initial surgical approach.
| Initial surgical approach | ||||
|---|---|---|---|---|
| Laparoscopic, N=97 (51.1%) | Open, N=93 (48.9%) | P | Conversion, N=35 (36.1%) | |
| Demographics | ||||
| Sex | 47 (48.5) male | 47 (50.5) male | 0.774 | 19 (54.3) male |
| Age (year) | 67.96 (15.82) | 68.38 (15.16) | 0.702 | 71.20 (12.29) |
| WHO performance index | 0.390 | |||
| 0 | 37 (38.1) | 26 (28.0) | 13 (37.1) | |
| 1 | 35 (36.1) | 33 (35.5) | 14 (40.0) | |
| 2 | 18 (18.6) | 27 (29.0) | 6 (17.1) | |
| 3 | 5 (5.1) | 5 (6.5) | 2 (5.7) | |
| 4 | 1 (1.0) | 1 (1.1) | - | |
| ASA classification | 0.003 | |||
| 1 | 13 (13.4) | 6 (6.5) | 5 (14.3) | |
| 2 | 58 (59.8) | 38 (40.9) | 19 (54.3) | |
| 3 | 23 (23.7) | 42 (45.2) | 9 (25.7) | |
| 4 | 3 (3.1) | 7 (7.5) | 2 (5.7) | |
| Charlson score | 3 [0–10] | 3 [0–11] | 0.172 | 3 [0–9] |
| 0 | 24 (24.7) | 29 (31.2) | 0.576 | 8 (22.9) |
| 1 | 9 (9.3) | 8 (8.6) | 4 (11.4) | |
| 2 | 16 (16.5) | 16 (17.2) | 5 (14.3) | |
| 3 | 26 (26.8) | 16 (17.2) | 10 (28.6) | |
| ≥4 | 22 (22.7) | 24 (25.8) | 8 (22.9) | |
| Number of previous ASBO | ||||
| 0 | 87 (89.7) | 84 (90.3) | 0.880 | 29 (82.9) |
| 1 | 8 (8.2) | 6 (6.5) | 1.000 | 4 (11.4) |
| 2 | 1 (1.0) | 2 (2.2) | 1.000 | 1 (2.9) |
| ≥3 | 1 (1.0) | 1 (1.1) | 1 (2.9) | |
| ≥Operative management | 5 (5.2) | 5 (5.4) | 4 (11.4) | |
| NOM only | 5 (5.2) | 5 (5.4) | 2 (5.7) | |
| Number of previous operations | 0.031 | |||
| 0 | 25 (24.7) | 10 (10.8) | 8 (22.9) | |
| 1 | 37 (38.1) | 35 (37.6) | 12 (34.3) | |
| 2 | 22 (22.7) | 23 (24.7) | 11 (31.4) | |
| ≥3 | 14 (14.4) | 25 (26.9) | 4 (11.4) | |
| ≥1 Laparotomy | 39 (40.2) | 67 (72.0) | 0.000 | 13 (37.1) |
| Laparoscopy only | 13 (13.4) | 5 (5.4) | 0.082 | 4 (11.4) |
| Type of previous surgery | ||||
| No abdominal surgery | 24 (24.7) | 10 (10.8) | 8 (22.9) | |
| Cholecystectomy | 3 (3.1) | 1 (1.1) | 1 (2.9) | |
| Gynecological with uterus extirpation | 5 (5.2) | 7 (7.5) | 1 (2.9) | |
| Gynecological no uterus extirpation | 6 (6.2) | 5 (5.4) | 3 (8.6) | |
| Liver | 0 | 0 | 0 | |
| Appendectomy | 16 (16.5) | 8 (8.6) | 4 (11.4) | |
| Urological | 2 (2.1) | 7 (7.5) | 0 | |
| Upper gastrointestinal | 4 (4.1) | 2 (2.2) | 1 (2.9) | |
| Retroperitoneal | 0 | 0 | 0 | |
| Other | 15 (15.5) | 26 (28.0) | 11 (31.4) | |
| Colon | 18 (18.6) | 20 (21.5) | 5 (14.3) | |
| Rectum | 4 (4.2) | 7 (7.5) | 1 (2.9) | |
| Operative outcomes | ||||
| Procedure | – | |||
| Adhesiolysis single adhesive band | 65 (67.0) | 51 (54.8) | 22 (62.0) | |
| Extensive adhesiolysis | 16 (16.5) | 19 (20.4) | 7 (20.0) | |
| Resection and anastomosis | 9 (9.3) | 9 (9.7) | 5 (14.3) | |
| Resection and stoma | – | 3 (3.2) | – | |
| Resection without stoma | 2 (2.1) | – | – | |
| Bypass | 2 (2.1) | 1 (1.1) | – | |
| Other | 5 (5.2) | 10 (10.8) | 1 (2.9) | |
| Duration of surgery (min) | 80.83 (45.2) | 82.52 (51.74) | 0.903 | 86.9 (51.68) |
| Serosasal injury | 29 (29.9) | 39 (41.9) | 0.084 | 14 (40.0) |
| Enterotomy | 13 (13.4) | 11 (11.8) | 0.744 | 6 (17.1) |
| Outcomes | ||||
| LOS (day) | 8.00 [0–109] | 11.00[1–129] | 0.000 | 9.00 [3–109] |
| ICU admission | 17 (17.5) | 24 (25.8) | 0.165 | 10 (28.6) |
| Duration (day) | 2.00 [1–35] | 1.00 [1–7] | 0.032 | 2.00 [1–35] |
| In-hospital mortality | 5 (5.2) | 4 (4.3) | 1.000 | 1 (2.9) |
| Readmission | 8 (8.2) | 15 (16.1) | 0.118 | 3 (8.6) |
| Complications | 3 (3.1) | 12 (12.9) | 0.071 | 1 (2.9) |
| Recurrence | 5 (5.2) | 3 (3.2) | 2 (5.7) | |
ASA, American Society of Anesthesiologists physical status classification; ASBO, adhesive small bowel obstruction; GE, gastroenterology; IC, intensive care; LOS, length of stay; NOM, nonoperative management; WHO, World Health Organization.
Table 4.
Demographic features and outcomes in patients treated surgically for adhesive small bowel obstruction (ASBO), based on the definitive surgical procedure.
| Definitive surgical approach | |||
|---|---|---|---|
| Laparoscopic, N=62 (32.6%) | Open, N=128 (67.4%) | P | |
| Demographics | |||
| Sex | 28 (45.2) male | 66 (51.6) male | 0.408 |
| Age (year) | 66.13 (17.33) | 69.15 (14.44) | 0.208 |
| WHO performance index | 0.660 | ||
| 0 | 25 (38.7) | 39 (30.5) | |
| 1 | 21 (33.9) | 47 (36.7) | |
| 2 | 12 (19.4) | 33 (35.8) | |
| 3 | 3 (4.8) | 8 (6.3) | |
| 4 | 1 (1.6) | 1 (0.8) | |
| ASA classification | 0.020 | ||
| 1 | 8 (12.9) | 11 (8.6) | |
| 2 | 39 (62.9) | 57 (44.5) | |
| 3 | 14 (22.6) | 51 (39.8) | |
| 4 | 1 (1.6) | 9 (7.0) | |
| Charlson score | 3 [0–10] | 3 [0–11] | 0.125 |
| 0 | 16 (25.8) | 34 (26.6) | 0.967 |
| 1 | 5 (8.1) | 12 (9.4) | |
| 2 | 11 (17.7) | 19 (14.8) | |
| 3 | 16 (25.8) | 25 (19.5) | |
| ≥4 | 14 (22.6) | 38 (29.7) | |
| Number of previous ASBO | 0.485 | ||
| 0 | 58 (93.5) | 113 (88.3) | |
| 1 | 4 (6.5) | 10 (7.8) | |
| 2 | 0 | 3 (2.3) | |
| ≥3 | 0 | 2 (1.6) | |
| ≥Operative management | 1 (1.6) | 9 (7.0) | 0.170 |
| NOM only | 3 (4.8) | 7 (5.5) | 1.000 |
| Number of previous operations | 0.136 | ||
| 0 | 16 (25.8) | 18 (14.2) | |
| 1 | 25 (40.3) | 47 (26.7) | |
| 2 | 11 (17.7) | 34 (36.6) | |
| ≥3 | 10 (16.1) | 29 (22.7) | |
| ≥1 Laparotomy | 26 (41.9) | 80 (62.5) | 0.008 |
| Laparoscopy only | 9 (14.5) | 9 (7.0) | 0.116 |
| Type of previous surgery | − | ||
| No abdominal surgery | 16 (25.8) | 18 (14.2) | |
| Cholecystectomy | 2 (3.2) | 2 (1.6) | |
| Gynecological with uterus extirpation | 4 (6.5) | 8 (6.3) | |
| Gynecological no uterus extirpation | 3 (4.8) | 8 (6.3) | |
| Liver | 0 | 0 | |
| Appendectomy | 12 (19.4) | 12 (9.4) | |
| Urological | 2 (3.2) | 7 (5.5) | |
| Upper gastrointestinal | 3 (4.8) | 3 (2.3) | |
| Retroperitoneal | 0 | 0 | |
| Other | 4 (6.5) | 37 (28.9) | |
| Colon | 13 (21.0) | 25 (19.5) | |
| Rectum | 3 (4.8) | 8 (6.3) | |
| Operative outcomes | |||
| Procedure | |||
| Adhesiolysis single adhesive band | 43 (69.4) | 73 (57.0) | – |
| Extensive adhesiolysis | 9 (14.5) | 26 (20.3) | |
| Resection and anastomosis | 4 (6.5) | 14 (10.9) | |
| Resection and stoma | – | 3 (2.3) | |
| Resection without stoma | 2 (3.2) | – | |
| Bypass | – | 1 (0.8) | |
| Other | 4 (6.5) | 11 (8.6) | |
| Duration of surgery (min) | 77.4 (41.1) | 83.7 (51.6) | 0.386 |
| Serosasal injury | 15 (24.2) | 53 (41.4) | 0.024 |
| Enterotomy | 7 (11.3) | 17 (13.2) | 0.818 |
| Outcomes | |||
| LOS (day) | 7.0 [0–28] | 10.5 [1–129] | 7.0 [0–28] |
| ICU admission | 7 (11.3) | 34 (26.6) | 0.023 |
| Duration (day) | 3 [1–12] | 1 [1–35] | 0.367 |
| In-hospital mortality | 4 (6.5) | 5 (3.9) | 0.477 |
| Readmission | 5 (8.1) | 18 (14.1) | 0.246 |
| Complications | 2 (3.2) | 13 (10.2) | 0.297 |
| Recurrence | 3 (4.8) | 5 (3.9) | |
ASA, American Society of Anesthesiologists physical status classification; ASBO, adhesive small bowel obstruction; GE, gastroenterology; IC, intensive care; LOS, length of stay; NOM, nonoperative management; WHO, World Health Organization.
Based on the intention-to-treat analysis, the laparoscopic and open groups were largely comparable at baseline. Patients in the open group had significantly higher ASA scores, more previous abdominal surgery, and more often one or more previous laparotomies (Table 3). Laparoscopy was more often performed in patients without previous abdominal surgery or with an appendectomy as only a previous surgical procedure. There were no differences in duration of surgery, ICU admission, readmission for complications or recurrent ASBO, and mortality between the open and intentional laparoscopic groups. Patients who underwent laparoscopic surgery had a shorter length of stay (8 vs. 11 days; P<0.001) compared with open surgery. ICU admissions were longer after laparoscopy (2.0 vs. 1.0 days; P=0.032). No significant difference was found regarding serosa injury (29/97 (29.9%) vs. 39/93 (41.9%); P=0.084) or a number of enterotomies (13/97 (13.4%) vs. 11/93 (11.8%); P=0.744). In-hospital mortality was higher for patients with an enterotomy compared with those without (4/24 (16.7%) vs. 5/166 (3.0%); P=0.003), but not for patients with serosal injury (6/122 (4.9%) vs. 3/68 (4.4%); P=0.875). Patients with serosal injuries or enterotomies did not have a longer hospital stay compared with patients without (serosal injury: 14.0 vs. 11.8 days; P=0.301 and enterotomy: 16.2 vs. 12.1 days; P=0.181). In the open group, extensive surgical procedures were performed more frequently, whereas, in the laparoscopic group, adhesiolysis of a single adhesive band was performed more frequently.
Patients treated laparoscopically scored 2 or more points on the Farinella criteria in 47.4%13, as compared with 75.3% of primarily open-treated patients. In the laparoscopic group, 20 patients (20.6%) with 2 or more points on the Farinella criteria were converted, as compared with 15 patients (15.5%) with 0 or 1 point. In 46% of laparoscopically treated patients with 2 or more points on the Farinella criteria, iatrogenic bowel injury occurred compared with 40% for patients with 0 or 1 point, with corresponding mortality rates of 2.0% and 5.7%, respectively.
Definitive surgical approach
Baseline characteristics between the definitive laparoscopic and open groups were comparable with the intention-to-treat analysis (Table 4). Successful laparoscopic surgery for ASBO was more often performed in patients with a virgin abdomen or an appendectomy as in previous surgical procedures. Length of stay was shorter in the laparoscopic group compared with the open group (7.0 vs. 10.5 days; P≤0.001). ICU admissions were less often required in the definitive laparoscopic group (11.3 vs. 26.6%; P=0.023). The laparoscopic group showed significantly less serosal injuries (24.2 vs. 41.4%; P=0.024), with a comparable proportion of enterotomies. In the open group, frequently more extensive surgical procedures were performed.
Timing of surgery
Operative management was performed in 71 (18.6%) patients within 24 h of admission. Delayed surgery was performed within 72 h from the start of NOM in 83 patients and after more than 72 h in 36 patients. There were no differences in baseline characteristics in patients who were operated on within 72 h from the start NOM compared with those who were operated on after 72 h from the start NOM. Hospital stays in patients who underwent delayed surgery was 10 days [2–129] and 17 days [6–109], respectively (P<0.001). Corresponding ICU admission rates (18.1 vs. 30.6%; P=0.130) and mortality rates were not significantly different (3.6 vs. 5.6%; P=0.638). Four recurrences of ASBO occurred in patients operated within 72 h from the start of NOM (4.8%), while none operated on after 72 h developed a recurrence within 90 days.
Discussion
Using a snapshot design, we were able to obtain an overview of the burden of ASBO and clinical practice from real-world data in the Netherlands. Patients receiving water-soluble contrast had a shorter hospital stay. Minimally invasive surgery as compared to open surgery was associated with shorter hospital stays and no differences in operative complications. However, the length of ICU stay was longer after minimally invasive surgery. Not solely the large number of inclusions but also the granularity of data regarding different diagnostics and treatment-related aspects during admission enables to explore knowledge gaps for potential improvement of clinical practice in ASBO.
A vast majority of patients in our study received same-day imaging, mostly a CT scan. This is according to the recommendations of the Bologna clinical practice guidelines10. Imaging by CT is a helpful tool to detect cases with another cause of obstruction than adhesions, which was 25% of SBO patients in our study. Previous studies reported that ~40% of all small bowel obstructions are not caused by adhesions1,19. In this study, we excluded patients with a known other cause of bowel obstruction, explaining the slightly higher rate of ASBO among patients in our study.
The number of patients undergoing emergency surgery in our study was relatively high; all patients undergoing emergency surgery had a CT scan. One in five patients with a first episode of ASBO underwent emergency surgery, as compared to less than 10% of patients with a recurrent episode. The relatively high number of patients, particularly those with a first episode of ASBO undergoing emergency, might partly be explained by a patient delay or delay in diagnosis from the onset of symptoms at first presentation. Another factor might be the 24/7 availability of specialized gastrointestinal surgeons in the Netherlands, lowering potential barriers for surgery in the emergency setting15,20,21.
As opposed to the high number of patients that received immediate imaging upon admission, only one in four patients received oral water-soluble contrast. There are numerous studies that have demonstrated diagnostic benefits of oral contrast and possibly also therapeutic benefits for NOM22,23. Also, in our study, the progression of contrast to the colon on follow-up imaging was predictive of successful NOM, and hospital stay was reduced in patients treated by NOM after receiving water-soluble contrast. Possibly, the option to administer oral contrast only after an initial CT scan with no oral contrast when a patient is initially treated by NOM is frequently overlooked. Water-soluble contrast increases the predictive value of follow-up imaging and might be therapeutic by its laxative aspects22,23. Thus, administering water-soluble contrast at the start of NOM can be beneficial, even if a CT scan has already been performed.
A trial of NOM has become the standard of care for ASBO without signs of ischemia nor peritonitis, or strangulation that requires emergency surgery. Benefits of NOM are low mortality and shorter hospital stay10. However, in recent years this standard of care has been debated because of the significantly higher risk of recurrence and multiple subsequent recurrences after NOM as compared with emergency surgery7,24. We indeed found a high recurrence of more than 15% after NOM within 90 days, which was three-fold higher than after surgery. Recurrences negatively impact long-term survival and quality of life25,26. Nevertheless, we demonstrated that the short-term morbidity of surgical treatment of ASBO should not be underestimated, and associated with considerable mortality of almost 5%, although the difference with NOM was not significant. In the British NELA report, 30-day mortality was even estimated at 7%6.
Performance of this Farinella criteria seemed quite poor in our data, as reflected by the minor differences in conversion rate, enterotomy, and mortality between the groups with a low and higher score on the Farinella criteria13. Thus it seems that the application of the Farinella criteria might withhold the benefits of laparoscopic surgery to a large group of patients.
A few limitations of this prospective nationwide cross-sectional need to be discussed. The study design in which centers are themselves responsible for the identification of potential candidates is that there is little data available on patients screened for eligibility. Nevertheless, the mix of urban and rural hospitals from all regions of the country implies that the study population is representative of Dutch ASBO patients. Furthermore, while universally accepted protocols for the management of ASBO are lacking, treatment allocation is made at the discretion of local protocols and preferences of the treating surgeon. Thus, treatment allocation might be subjected to selection bias, and we indeed found a few baseline differences between the groups. This observational study has been pivotal in revealing areas of practice variation and future research. However, the observational nature of this study precludes drawing firm conclusions on the superiority of different treatment strategies.
An important topic for future research will be the reduction of recurrences. Although the follow-up in our study was only 90%, a high risk of recurrence was registered, especially after NOM. The incidence of recurrence is expected to rise further with longer follow-up, as new cases continue to occur many years after the initial episode. In our study, there was no difference in short-term risk of recurrence compared between open and laparoscopic surgery, but studies with long-term results are still lacking. Also, comparative studies on the efficacy of elective adhesiolysis and adhesion barriers for recurrent ASBO are awaited. Areas for potential improvement of practice variation include the use of oral contrasts in NOM and the use of adhesion barriers in surgically treated cases.
Conclusion
Results of this nationwide cross-sectional study demonstrated a high burden of ASBO, with overall 3% mortality and a median of 8 days of hospitalization. Minimally invasive surgery for ASBO was not associated with an increased risk of mortality or iatrogenic injuries. Operating patients after failure of NOM within 72 h was associated with a shorter hospital stay. WSC use and the use of minimally invasive techniques were also associated with a decreased length of hospital stay. Additional intervention studies are required to determine the specific role of these interventions in a standardized approach toward the management of ASBO.
Ethical approval
The medical ethical committee of Radboud University Medical Center in Nijmegen reviewed and approved this study (2018-4214).
Sources of funding
No funding was received for this study.
Author contribution
P.K.: substantial contributions to the conception and design of the work, analysis and interpretation of data, drafting the work and revising it critically for important intellectual content, final approval of the version to be published, agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
L.P.A.K.: substantial contributions to the analysis and interpretation of data, drafting the work and revising it critically for important intellectual content, final approval of the version to be published, agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
M.W.J.S., P.J.T., J.J.W., J.M., R.R., and E.M.G.B.: substantial contributions to the conception and design of the work, revising the work critically for important intellectual content, final approval of the version to be published, agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
N.D.B.: substantial contributions to the analysis and interpretation of data, revising the work critically for important intellectual content, final approval of the version to be published, agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
H.vG. and R.P.G.tB.: substantial contributions to the conception and design of the work, the analysis and interpretation of data, revising the work critically for important intellectual content, final approval of the version to be published, agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
ASBO Snapshot Study Group: substantial contributions to the collection of data, the analysis and interpretation of data, revising the work critically for important intellectual content, final approval of the version to be published, agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Conflicts of interest disclosure
The authors have no conflicts of interest to declare.
Research registration unique identifying number (UIN)
Name of the registry: clinicaltrials.gov.
Unique identifying number or registration ID: NCT03786159.
Hyperlink to your specific registration (must be publicly accessible and will be checked): National Snapshot Study Adhesive Small Bowel Obstruction (ASBO) – Full-Text View – ClinicalTrials.gov.
Guarantor
P.K., M.W.J.S., N.D.B., P.J.T., H.vG., and R.P.G.tB.
Data availability statement
The data that support the findings of this study are available on request from the corresponding author (P.K.). The data are not publicly available due to their containing information that could compromise the privacy of research participants.
Provenance and peer review
Not commissioned, externally peer-reviewed.
Acknowledgements
ASBO Snapshot Study Group
P.A. Neijenhuis4, S. Vogels4, M.P.A. Bus4, J.B. Tuynman5, L.S. Boogerd5, R. Detering5, R.M.P.H. Crolla6, K. de Leur6, R.M. Smeenk7, C.A.L. de Raaff7, W. van der Meij8, N.E. de Jong8, F. Polat9, N. Smakman10, K.M. Govaert10, D.J.A. Sonneveld11, R.J.S. Coelen11, T.W.A. Koedam11, A.K. Talsma12, K. Degenaar12, B.P.L. Wijnhoven3, J.L.A. van Vugt3, A.E. Taselaar3, Dr. M.S. Ibelings13, Drs. M.W. Jolles13, Dr. B.J. Noordman14, S. van Egmond14, M.M. Poelman14, P. van Duijvendijk15, D. Reetz15, G.J.D. van Acker16, M.K. Toneman1,16, A.E. van der Pool16, J. Nonner17, A.S. de Boer17, H.L. van Westreenen18, B.A. de Cort18, A.Q. van Hoesel18, J. Heemskerk19, J.C.A. Hardy19, Prof. Dr. E.C.J. Consten20,35, T.A. Burghgraef20, M.P.C.M. Smit20, K.W. van Dongen21, E. van Duyn22, B.A. van den Beukel22, A.G.W.E. Wintjes2, S.M.M. de Castro23, S.C. Kleipool23, J.K. Wiggers23, J.W.T. Dekker24, G.M. Struik24, B. Inberg25, R. Silvis26, A.M. Dinaux26, T. Verhaak26, B. Wiering27, D.P.J. Smeeing27, E. Westerduin28, A.A.W. van Geloven28, T. van Asbeck28, J. Beutler28, W.M.U. van Grevenstein29, J.J.E.M. van Laarhoven29, J.L.M. Konsten30, S. Bessems30, Dr. M.F. Lutke Holzik31, A. Cosovic31, E.G. Boerma32, M.L.G. Vane32, F.C. den Boer33, M. Pape33, J.T. Heikens34, E. Schat34. 1Department of Surgery, Radboud University Medical Center, Nijmegen, The Netherlands. 2Department of Surgery, Maastricht University Medical Center, Maastricht, The Netherlands. 3Department of Surgery, Erasmus Medical Centre, Rotterdam, The Netherlands. 4Department of Surgery, Alrijne Hospital, Leiderdorp, The Netherlands. 5Department of Surgery, Amsterdam University Medical Centres, Amsterdam, The Netherlands. 6Department of Surgery, Amphia Hospital, Brede, The Netherlands. 7Department of Surgery, Albert Schweitzer Hospital, Dordrecht, The Netherlands. 8Department of Surgery, Bernhoven Hospital, Uden, The Netherlands. 9Department of Surgery, Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands. 10Department of Surgery, Diakonessenhuis, Utrechts, The Netherlands. 11Department of Surgery, Dijklander Hospital, Hoorn, The Netherlands. 12Department of Surgery, Deventer Hospital, Deventer, The Netherlands. 13Department of Surgery, Elisabeth-TweeSteden Hospital, Tilburg, The Netherlands. 14Department of Surgery, Fransiscus Gasthuis, Rotterdam, The Netherlands. 15Department of Surgery, Gelre Hospital, Apeldoorn, The Netherlands. 16Department of Surgery, Haaglanden Medical Center, Leidschendam, The Netherlands. 17Department of Surgery, Ikazia Hospital, Rotterdam, The Netherlands. 18Department of Surgery, Isala, Zwolle, The Netherlands. 19Department of Surgery, Laurentius Hospital, Roermond, The Netherlands. 20Department of Surgery, Meander Medical Center, Amersfoort, The Netherlands. 21Department of Surgery, Maas Hospital Pantein Boxmeer, Boxmeer, The Netherlands. 22Department of Surgery, Medisch Spectrum Twente, Enschede, The Netherlands. 23Department of Surgery, OLVG Hospital, Amsterdam, The Netherlands. 24Department of Surgery, Reinier de Graaf Gasthuis, Delft, The Netherlands. 25Department of Surgery, Queen Beatrix Medical Center, Winterswijk, The Netherlands. 26Department of Surgery, Spaarnegasthuis, Hoofddorop, The Netherlands. 27Department of Surgery, Slingeland Hospital, Doetinchem, The Netherlands. 28Department of Surgery, Tergooi Medical Center, Hilversum, The Netherlands. 29Department of Surgery, Univeristy Medical Center Utrecht, Utrecht, The Netherlands. 30Department of Surgery, Viecuri Medical Center, Venlo, The Netherlands. 31Department of Surgery, Ziekenhuisgroep Twente, Almelo, The Netherlands. 32Department of Surgery, Zuyderland Medical Center, Heerlen and Sittard/Geleen, The Netherlands. 33Department of Surgery, Zaans Medical Center, Zaandam, The Netherlands. 34Department of Surgery, Rivierenland Hospital, Tiel, The Netherlands. 35Departement of Surgery, University Medical Center Groningen, Groningen, The Netherlands.
Supplementary Material
Footnotes
Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.
Published online 5 June 2023
Contributor Information
Pepijn Krielen, Email: pepijn.krielen@radboudumc.nl.
Lisa P.A. Kranenburg, Email: l.kraneburg@student.maastrichtuniversity.nl.
Martijn W.J. Stommel, Email: martijn.stommel@radboudumc.nl.
Nicole D. Bouvy, Email: n.bouvy@mumc.nl.
Pieter J. Tanis, Email: p.tanis@erasmusmc.nl.
Jorn J. Willemsen, Email: jornwillemsen@gmail.com.
Jorne Migchelbrink, Email: jorne.migchelbrink@radboudumc.nl.
Rick de Ree, Email: Rick.d.ree@live.nl.
Esther M.G. Bormans, Email: Esther.bormans@hotmail.com.
Harry van Goor, Email: harry.vangoor@radboudumc.nl.
Richard P.G. ten Broek, Email: richard.tenbroek@radboudumc.nl.
Collaborators: P.A. Neijenhuis, S. Vogels, M.P.A. Bus, J.B. Tuynman, L.S. Boogerd, R. Detering, R.M.P.H. Crolla, K. de Leur, R.M. Smeenk, C.A.L. de Raaff, W. van der Meij, N.E. de Jong, F. Polat, N. Smakman, K.M. Govaert, D.J.A. Sonneveld, R.J.S. Coelen, T.W.A. Koedam, A.K. Talsma, K. Degenaar, B.P.L. Wijnhoven, J.L.A. van Vugt, A.E. Taselaar, Dr M.S. Ibelings, Drs M.W. Jolles, B.J. Noordman, S. van Egmond, M.M. Poelman, P. van Duijvendijk, D. Reetz, G.J.D. van Acker, M.K. Toneman, A.E. van der Pool, J. Nonner, A.S. de Boer, H.L. van Westreenen, B.A. de Cort, A.Q. van Hoesel, J. Heemskerk, J.C.A. Hardy, E.C.J. Consten, T.A. Burghgraef, M.P.C.M. Smit, K.W. van Dongen, E. van Duyn, B.A. van den Beukel, A.G.W.E. Wintjes, S.M.M. de Castro, S.C. Kleipool, J.K. Wiggers, J.W.T. Dekker, G.M. Struik, B. Inberg, R. Silvis, A.M. Dinaux, T. Verhaak, B. Wiering, D.P.J. Smeeing, E. Westerduin, A.A.W. van Geloven, T. van Asbeck, J. Beutler, W.M.U. van Grevenstein, J.J.E.M. van Laarhoven, J.L.M. Konsten, S. Bessems, M.F. Lutke Holzik, A. Cosovic, E.G. Boerma, M.L.G. Vane, F.C. den Boer, M. Pape, J.T. Heikens, and E. Schat
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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 data that support the findings of this study are available on request from the corresponding author (P.K.). The data are not publicly available due to their containing information that could compromise the privacy of research participants.