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Gastrointestinal Imaging |
1 The complete list of investigators and affiliations is listed at the end of this article. Received June 15, 2005; revision requested August 15; revision received February 10, 2006; accepted March 6; final version accepted July 13. Supported by a grant from the European Association of Radiology administered by the European Society of Gastrointestinal and Abdominal Radiology and a Kodak Scholarship administered by the Royal College of Radiologists, United Kingdom. Address correspondence to Steve Halligan, MD, FRCP, FRCR, Department of Radiology, University College London, Level 2 Podium, 235 Euston Rd, London NW1 2BU, England (e-mail: s.halligan{at}ucl.ac.uk).
| ABSTRACT |
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Materials and Methods: Physicians at each participating center received ethical committee approval and followed the committees' requests regarding informed consent. Nine experienced radiologists, nine trained radiologists, and 10 trained technologists from nine centers read 40 CT colonographic studies selected from a data set of 51 studies and modeled to simulate a population with positive fecal occult blood test results: Studies were obtained in eight patients with cancer, 12 patients with large polyp, four patients with medium polyp, and 27 patients without colonic lesions. Findings were verified with colonoscopy. An experienced radiologist used 50 endoscopically validated studies to train novice observers before they were allowed to participate. Observers used one software platform to read studies over 2 days. Responses were collated and compared with the known diagnostic category for each subject. The number of correctly classified subjects was determined for each observer, and differences between groups were examined with bootstrap analysis.
Results: Overall, 28 observers read 1084 studies and detected 121 cancers, 134 large polyps, and 33 medium polyps; 448 healthy subjects were categorized correctly. Experienced radiologists detected 116 lesions; trained radiologists and technologists detected 85 and 87 lesions, respectively. Overall accuracy of experienced observers (74.2%) was significantly better than that of trained radiologists (66.6%) and technologists (63.2%). There was no significant difference (P = .33) between overall accuracy of trained radiologists and that of technologists; however, some trainees reached the mean performance achieved by experienced observers.
Conclusion: Experienced observers interpreted CT colonographic images significantly better than did novices trained with 50 studies. On average, no difference between trained radiologists and trained technologists was found; however, individual performance was variable and some trainees outperformed some experienced observers.
© RSNA, 2007
| INTRODUCTION |
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At the time of this writing, there were no evidence-based guidelines for training; however, a working group suggested that supervised interpretation of at least 40 validated studies might be adequate for this purpose (7). However, when this suggestion was tested on a small scale, it was shown that observer response to such training is highly unpredictable and that performance may even deteriorate (8). Also, a recent study revealed that some novice observers exposed to a training module could outperform their more-experienced colleagues (9).
The European Society of Gastrointestinal and Abdominal Radiology is interested in developing evidence-based guidelines for training and accrediting radiologists in the interpretation of CT colonographic studies. With this goal in mind, the purpose of our study was to define the interpretative performance of radiologists with experience in CT colonography and to compare their performance with that of novice observers who had undergone directed training, with colonoscopy serving as the reference standard.
| MATERIALS AND METHODS |
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Data Set Composition and Accrual
We collated a data set of normal and abnormal CT colonographic studies submitted by the seven participating centers. In this data set, prevalence and morphology of neoplasia were modeled to simulate those expected in patients with positive fecal occult blood test results (prevalence of cancer, 10%; prevalence of large polyps, 30%; prevalence of medium polyps, 10%; prevalence of normal colorectum, 50%) (1012). The aim of this procedure was to create a mix of studies with normal and abnormal findings to investigate sensitivity for different classes of neoplasia and specificity between observer groups. This mix also ensured that the data set was clinically relevant.
Physicians at each center were asked to submit 10 studies that were obtained in subjects aged 5069 years and that matched the expected prevalence of neoplasia on the basis of fecal occult blood test results (ie, one patient with cancer, three patients with large polyps, one patient with medium polyps, and five subjects with no colonic lesion) (1012). The four diagnostic categories were as follows: cancer, large polyps, medium polyps, and normal. In line with the results of fecal occult blood test trials, a large polyp was defined as a polyp measuring 10 mm or more in diameter and a medium polyp was defined as a polyp measuring less than 10 mm in diameter (69 mm in diameter for the purposes of this study).
To reflect normal variation in data quality, subjects from each center were recruited in a strictly chronologically consecutive fashion. That is to say, consecutive subjects were assigned to an appropriate diagnostic category until all four categories were full. Thus, the first patient with cancer completed recruitment to this category, whereas three consecutive patients with large polyps were necessary to complete recruitment to this category. Patients with multiple lesions were assigned to a category according to the largest lesion detected, which was referred to as the index lesion. To ensure that studies accurately reflected the natural and inevitable technical variation found in day-to-day practice, centers were obliged to submit all eligible studies, with the exception of those that were deemed nondiagnostic (ie, any study in which the local principal investigator would normally recommend repeat colonography or another examination because of insurmountable technical problems, such as segmental collapse or retained fluid). In all subjects, CT findings were defined by subsequent same-day colonoscopic findings obtained by experienced practitioners. Polyp size was based on the colonoscopic measurement, which was estimated with adjacent biopsy forceps.
Participating centers were chosen because they had active CT colonography research programs at the time the study protocol was developed and because they could contribute studies. We also stated that as long as studies were chronologically consecutive, centers could submit retrospective studies, provided the technical stipulations for CT colonography were satisfied. Five centers submitted only retrospective data, and two centers submitted only prospective data. Ethical permission for data sharing was covered by the local stipulations at each center. Four centers that submitted retrospective data did not require additional specific ethical committee approval for this study because data were collected as part of a local study, and ethical committee approval and patient informed consent were applicable for additional analyses and data sharing. The fifth center that submitted retrospective data obtained ethical committee approval and verbal consent via telephone from the subjects selected. Physicians at the two centers that submitted prospective data obtained patient informed consent, ethical committee approval, and permission for additional analyses and data sharing with ongoing studies, provided patient identifying information was removed before data sharing. We applied this stipulation to all data collected for this study.
Images were acquired with the patient in the prone and supine positions with full bowel purgation, a collimation that was no greater than 2.5 mm, and use of a multidetector row CT scanner. Gas insufflation and spasmolytic use were left to the discretion of local physicians. Low-radiation-dose protocols were permissible, but administration of intravenous contrast material was impermissible on the grounds that contrast agents are unlikely to be used in a screening program. Fecal tagging was not permitted since this procedure was not common practice at the time of data accrual (May to November 2003). Studies were archived on a compact disk and transferred to the trial office; technical and diagnostic category data were included for each study.
Of the seven centers that submitted data, three provided data only from symptomatic patients, one provided data only from asymptomatic patients, and three provided data from both symptomatic and asymptomatic patients. Four centers submitted studies obtained in a full data set of 10 subjects; however, the file containing one study could not be opened at the trial office. The three remaining centers submitted five, four, and three studies because of difficulties satisfying protocol requirements, notably, those related to age. Thus, our study included 51 subjects, of whom 27 (53%) had no colonic lesion and 24 (47%) had an index lesion. Of the 24 patients with an index lesion, eight had cancer, 12 had large polyps, and four had medium polyps. Seven (29%) of the patients with an index lesion had a second lesion: Two patients with cancer each had an additional large polyp, and one patient with cancer and four patients with large polyps each had an additional medium polyp.
Observers
The data set was interpreted by the following three groups of observers: experienced radiologists and trained radiologists and radiologic technologists. Nine centers (including all seven that submitted imaging studies) provided an observer for each group; one center provided two technologists.
An experienced radiologist was defined as a radiologist who had considerable practical and/or research experience with CT colonography prior to this study. Individual experience ranged from evaluation of 325 to evaluation of 1200 studies (median, 750 studies), with between 120 and 600 studies (median, 200 studies) validated with colonoscopy.
Each experienced radiologist identified a local radiologist and radiologic technologist who had interpreted 10 or fewer studies prior to this study. We stipulated that radiologists be familiar with the interpretation of standard abdominopelvic CT studies and that technologists be familiar with the acquisition of abdominopelvic CT studies. The experienced radiologists used normal and abnormal studies that had been acquired locally and verified with subsequent colonoscopy to train inexperienced radiologists and technologists to interpret CT colonographic images. There was no attempt to use the same training data set at all participating centers because we wanted to emulate existing training programs for conventional CT (in which trainees generally learn by using studies acquired locally). However, we did stipulate that 50 individual studies should be interpreted; interpretation was to be unaided initially and then followed by face-to-face discussion with the local trainer on a patient-by-patient basis, so as to closely mimic standard day-to-day training practice. Trainers and trainees used the preferred local reading platform, in line with everyday practice. We stipulated that training should occur over several separate sessions and several weeks to reflect standard teaching practice.
Reading Conditions and Outcome Measures
After training, an individualized test data set of 40 studies was prepared by the trial coordinator for each participating center. These 40 studies were sampled from the data set of 51 studies and balanced in terms of the prevalence of abnormalities; studies submitted by a center were excluded from the data set sent to that center. The order of studies was randomized to mix abnormal and normal cases, and all readers read the studies in the same order. All patient identifiers were removed. The experienced radiologist (n = 9), trained radiologist (n = 9), and trained technologist(s) (n = 10) at each center then interpreted this data set over 2 days. The trial coordinator visited each center to supervise reading, which was conducted with individual laptop computers equipped with 17-inch (43.18-cm) screens and software that allowed a primary two-dimensional analysis, with three-dimensional analysis available for problem solving (Voxar ColonScreen, version 2.2; Barco, Edinburgh, Scotland). Observers were familiarized with the software, when necessary, and the supervisor was available at all times. Reading was performed in a quiet environment with ambient light. Observers were asked to read at their own pace, with no requirement to finish within a prespecified time. Observers had read the study protocol and knew that studies obtained at their own institutions (if any) had been excluded, but they had no specific information about the composition of their individualized data set.
Observers used a data sheet to categorize each subject as either healthy or unhealthy. Subjects designated as unhealthy were further categorized as having cancer, a large polyp, or a medium polyp. Large polyps had a maximal two-dimensional transverse diameter of 10 mm or larger, whereas medium polyps had a diameter of 69 mm; software calipers were used to obtain these measurements. Observers noted any polyp that measured 5 mm or less but categorized subjects with such polyps as healthy; this practice allowed false-negative findings due to measurement error to be distinguished from false-negative findings due to perceptual error. Observers were unaware of each other's responses. Prone and supine image coordinates and segmental location were recorded for each perceived abnormality so that false-positive responses could be distinguished from true-positive responses in the same patient. Multiple responses were possible. There were six bowel segments (rectum, sigmoid colon, descending colon, transverse colon, ascending colon, and cecum), and observers were provided with an annotated diagram of segmental definitions. Observers were free to classify a study as technically inadequate, although steps had been taken when designing the study protocol to avoid including nondiagnostic studies.
Data sheets were collated, and observers' responses were compared with the known diagnostic category. The trial coordinator (who had experience with more than 300 endoscopically verified studies) independently evaluated each study to confirm both the CT findings reported by the submitting center and the CT coordinates of the abnormality, which were then used to determine whether observers' responses were true-positive or false-positive. All but one of the endoscopically validated lesions could be identified. However, observers encountered difficulty locating four flat adenomas (which measured 40, 30, 15, and 12 mm in diameter), one of which was only visible when standard abdominal CT window settings were used (window level, 40 HU; window width, 400 HU) (Fig 1). One flat adenoma (40 mm) could not be identified despite good bowel preparation and distention and a thorough review of endoscopic data.
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Two measures were derived for each reader: sensitivity for lesions (number of lesions correctly seen divided by number of lesions present) and accuracy (the overall percentage of correct categorizations). For both measures, studies classified as technically inadequate by readers were included. For the most part, observers read the same studies and observations were correlated to some extent; therefore, a bootstrap analysis was used to investigate differences between observer groups. A total of 1999 samples were redrawn randomly from the original sample, with replacement and analysis of each resultant data set. The results of interest were calculated for each bootstrap sample, and the distribution of values was used to obtain a bootstrap confidence interval. A probability value was also calculated by considering how many of the values were farther from zero than the actual value observed with the data. Results were considered statistically significant at a probability level of 5%. Statistical analysis was performed with Stata, version 8.0, software (Stata, College Station, Tex).
| RESULTS |
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Overall, 736 (68%) patients were correctly classified (Table 1). The number of lesions correctly classified declined in conjunction with decreased size of the index lesion: Cancer was detected in 121 (79%) patients, large polyps were detected in 134 (47%), and medium polyps were detected in 33 (36%) (Table 1). In the remaining 348 patients, the index lesion was missed in 239, findings were false-positive in 73, and studies were deemed technically inadequate in 36. Of the 36 technically inadequate studies, 23 (64%) related to one subject who had no colonic lesion. Of the 13 other technically inadequate studies, 11 related to subjects who had no colonic lesion. Overall, the false-positive rate was 13% (22 of 176 studies) for experienced radiologists, 12% (21 of 169 studies) for trained radiologists, and 16% (30 of 188 studies) for technologists. One experienced radiologist and two technologists did not assign any false-positive diagnoses. Six readers (one experienced observer, two radiologists, and three technologists) had false-positive rates of 20% or more.
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| DISCUSSION |
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However, it could be argued that our proposition that trainees should achieve the competence of experienced observers is flawed. A distinction can be made between "best achievable" and "acceptable" performance. On average, subspecialist radiologists perform better than their generalist peers because subspecialists are able to make decisions on the basis of prior experience (13). Whether all radiologists interpreting CT colonographic studies need to be as capable as those with extensive experience is a question to be answered by the wider radiologic community. The answer will depend on whether the examination is performed by generalists or subspecialists. A number of observations will indicate this. First, subspecialization has affected radiology since the 1920s (14); since then, it has become more prevalent for a number of reasons, not the least of which is that it is thought to benefit patients (15). The ultimate position of CT colonography as a specialist examination is thus more likely today than it was previously. A parallel may be drawn with a barium enema examination, which is widely considered a general examination despite compelling evidence that interpretation of barium enema studies is best handled by those with extensive experience (16). Furthermore, since the inception of CT colonography, the diagnostic performance of this modality has been compared with that of colonoscopy, which is reportedly a more effective test than a barium enema examination (17). Comparisons between skilled colonoscopists and less-skilled colonographers damage the reputation of CT colonography (18).
It may be possible to stratify acceptable performance contingent on the clinical setting. For example, it has been argued that for mammography, the highest aptitude is necessary for screening because patients are asymptomatic and lesions are often difficult to detect (19). The same principle might apply to CT colonography. Like mammography, colonography may be used to examine symptomatic patients (who actually constitute the largest group that undergoes this procedure in research studies). Symptomatic colonic lesions tend to be larger and easier to detect than asymptomatic lesions; thus, it may be possible that less interpretative skill is needed to detect symptomatic lesions. This hypothesis is supported by our findings, which show that detection rates increased in line with lesion size for all observer groups. However, while cancers were the easiest index lesions for the trained observers to detect, whether a potential patient or health-policy maker would be satisfied with a 70% average detection rate is a subject for wider debate.
It was not the aim of our study to investigate the performance characteristics of CT colonography. Rather, we aimed to determine the performance of novice observers relative to that of experienced observers after novice observers had undergone training with a schedule that was in line with proposed guidelines (7). With this approach, no aspect of individual aptitude is taken into account. It is inevitable that some individuals will outperform others despite similar professional backgrounds and training. Our data revealed considerable overlap in individual performance between all groups. Notably, there were two trained radiologists and one trained technologist whose accuracy exceeded the mean accuracy achieved by the experienced observers. Conversely, the accuracy of one experienced observer was below the mean accuracy achieved by both trained groups, even after difficult-to-detect lesions were excluded. Our data suggest that competence might be achieved by certain talented individuals after they complete a training program based on 50 validated studies. Merely completing such training is insufficient to guarantee competency, and it is self-evident that competent individuals will need to be identified in some other way, possibly with an examination. Again, this is a subject for wider debate. It should be noted that because our sample data set was relatively small, the observed variability between observers will likely exceed the real variability because of sampling error. A larger study would likely reveal performance that regressed toward the mean value for each group. Because of this, it would be unwise to overemphasize the performance of individuals in the present study.
Considering aptitude further, on average, we found no difference between the trained radiologists and the trained technologists, despite the radiologists' relative wealth of interpretative experience with CT. Also, the range of individual abilities was similar between these two groups. This suggests that the paradigm for interpretation of CT colonographic studies differs from that for interpretation of routine CT studies; thus, radiologists may not have an intrinsic advantage (unless we also consider the detection of extracolonic lesions, which we chose not to address). This may be explained by the fact that one organ is being examined for one disease (ie, neoplasia); therefore, an extensive medical knowledge base confers no substantial advantage. Furthermore, the skills required for colonic navigation are different from those used to interpret conventional CT studies, and interpretation takes longer, with a greater potential for observer fatigue and error (20). Our data possibly support the concept that radiographic technologists may be a valuable resource for interpretation of studies, especially when radiologists are in short supply. This is already the case for interpretation of barium enema studies, and it is a cost-effective measure (21,22).
Although our primary aim was to assess the relative performance of experienced and trained observers, we should explore the reasons behind the overall detection rate of only 57% of large polyps, which lags behind that in some studies (23) and meta-analyses (24,25). This was undoubtedly influenced by the disproportionately high percentage of flat adenomas (a third of large polyps were flat, and one was invisible on CT images, even in retrospect), and it may not translate to series that are more representative of the general population. The findings of large series in which dye-spray colonoscopy was used suggest that 13%15% of large adenomas are flat (26,27). Ironically, the higher percentage of flat adenomas in our study was a result of our attempts to make the data set reflect conditions in everyday practice. We prevented investigators from submitting only their best studies by stipulating that studies be accrued in a chronologically consecutive fashion. Some contributing centers had ongoing research relating to hereditary cancer, which increased the prevalence of flat lesions in our study. The consequence of this was twofold: Most obviously, detection rates were reduced. Also, flat adenomas diminished our power to discriminate between groups because they present a challenge to all observers (28). However, they can be detected if observers are careful in their interpretation (28); for example, one experienced observer identified two flat adenomas. The proportion of flat adenomas should be reported in future studies of CT colonography.
Our study did have limitations. We originally intended that all participating centers would contribute studies obtained in 10 patients; however, not all centers did this. Three centers did not contribute any studies because they could not satisfy protocol stipulations.
Although the data set was designed to reflect what might be expected in a fecal occult blood test screening program, it was by necessity a simulation and can be regarded as a convenience sample. Assumptions for the bootstrap analysis best suit a random sample. For example, cancers detected at screening are in an earlier stage than those that are detected in patients who present with symptoms (1012). Conversely, adenomas detected with the fecal occult blood test are larger than those in asymptomatic patients (1012). We have discussed the difficulties posed by the proportion of flat adenomas.
Reading conditions were, by necessity, artificial. Image interpretation induces fatigue (6), and practitioners are currently unlikely to read 20 studies per day. However, this was a pragmatic necessity for this study, and this paradigm has been adopted successfully in other high-profile studies that have involved large numbers of observers from several centers (6). Our original intention was for observers to use their preferred software platform, but difficulties uploading studies prevented this. Instead, we assembled the data set onto laptop computers that could be transported easily to each center. These computers had high-resolution screens, and the software used a two-dimensional approach, with a three-dimensional approach available for problem solving; this was the preferred method of analysis for the majority of experienced readers at the time of the study. All normal software functions were preserved on the computers. Because some readers had been trained to use another platform locally, we ensured that the software used in this study was easy to learn, and the study supervisor was available at all times to help, if necessary. While there is some evidence that the type of software platform used does not influence accuracy (6), it is possible that accuracy may have improved if a primary three-dimensional approach had been available (23). However, it should be stressed that we aimed to investigate the relative performance of observers and not the confounding effect of the software platform. Whether the reading platform used has a differential effect on experienced observers versus trained readers clearly merits further research. The use of laptop computers also meant that study loading times were longer than those of a workstation, and this may have frustrated some readers.
Investigators have examined the effect of implementing an identical training schedule for novice observers, with use of a teaching file and test set (29); however, we decided to leave the patient selection and training schedule largely to the discretion of the local trainer (beyond stipulations relating to the number of studies and length of training) because we thought this would better reflect current teaching practice. As a result, differences in performance potentially could be explained by variations in the quality of local training, which are precisely what occur in residency programs in general. For example, some trainers may have emphasized the importance of careful soft-tissue reading when looking for flat lesions, whereas other trainers may not have stressed this point. Whether an identical training scheme and materials administered via a training course are superior to more prolonged but less standardized local training is a subject that needs further investigation.
We have already stated that because our data set was relatively small, observed variability between readers may have been increased. Also, not all observers read the same studies to prevent recall bias due to interpretation of studies obtained at an observer's own center; however, we did balance the prevalence of abnormalities across all data sets so that they would remain comparable.
In conclusion, experienced observers asked to interpret CT colonographic studies performed significantly better on average than did novice observers who were trained with 50 endoscopically validated studies. However, individual performance is variable, and some trainees may outperform some experienced radiologists. On average, we found no performance difference between trained radiologists and trained radiographic technologists, which suggests that prior interpretation of conventional abdominal CT studies may not be of benefit for interpretation of CT colonographic studies.
European Society of Gastrointestinal and Abdominal Radiology (ESGAR) CT Colonography Study Group Investigators:
Principal investigator: Steve Halligan, FRCR (University College London). Trial coordinator and data manager: David Burling, FRCR (St Mark's Hospital, London, England). Writing committee: Steve Halligan, FRCR; David Burling, FRCR, Wendy Atkin, PhD, and Clive Bartram, FRCR (St Mark's Hospital); Helen Fenlon, MD (Mater Misericordiae University Hospital, Dublin, Ireland); Andrea Laghi, MD (La Sapienza, Rome, Italy); and Jaap Stoker, MD (Amsterdam Medical Centre, Amsterdam, the Netherlands). Statisticians: Douglas G. Altman, DSc (Cancer Research UK/NHS Centre for Statistics in Medicine, Wolfson College, Oxford, England) and Paul Bassett, BSc (Statistical Consultant, Ruislip, Middlesex, England). ESGAR liaison: Roger Frost, FRCR (Salisbury NHS Trust, Salisbury, England). Study readers and local coordinators: Stuart Taylor, FRCR (University College London); Clive Bartram, FRCR, Lesley Honeyfield, DCR, and Melinda De Villiers, DCR (St Mark's Hospital); David Nicholson, FRCR, Velauthan Rudralingham, FRCR, and Lisa Renaut, DCR (Hope Hospital, Salford, England); Clive Kay, FRCR, Andy Lowe, FRCR, and Jane Williams-Butt, DCR (Royal Infirmary, Bradford, England); Jasper Florie, MD, and Martin Poulus (Academic Medical Center, Amsterdam, the Netherlands); Victor Van der Hulst, MD (Onze Lieve Vrouwe Gasthuis, Amsterdam, the Netherlands); Philippe Lefere, MD, Jesse Marrannes, and Guido Dessey, MD (Stedelijk Ziekenhuis, Roeselare, Belgium); Helen Fenlon, MD, Alan O'Hare, MD, and Shane Foley (Mater Misericordiae University Hospital, Dublin, Ireland); Emmanuele Neri, MD, Paola Vagli, MD, and Benedetta Politi (University of Pisa, Pisa, Italy); Riccardo Iannaccone, MD, Filipo Mangiapane, MD, and Sante Ori (La Sapienza, Rome, Italy); and Teresa Gallo, MD, Giulia Nieddu, MD, Saverio Signoretta, and Daniele Regge, MD (Candiolo Oncologic Hospital, Turin, Italy).
| ADVANCES IN KNOWLEDGE |
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| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, S.H., D.B.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, S.H., D.B., W.A.; clinical studies, S.H., D.B., H.F., R.F., S.T., D.N., J.W.B., J.F., M.P., V.V.d.H., P.L., J.M., G.D., A.O., S.F., E.N., P.V., R.I., F.M., D.R.; statistical analysis, S.H., D.G.A., P.B.; and manuscript editing, S.H., D.B., W.A., C.B., H.F., A.L., J.S.
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