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Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

Objective

To introduce and evaluate a new standardized ultrasound (US) score developed for large joints in patients with rheumatoid arthritis (RA).

Methods

A US score was designed to determine the degree of inflammation in the shoulder, the elbow, the hip, and the knee joint in patients with RA (Sonography of Large Joints in Rheumatology [SOLAR] score). Synovitis and synovial vascularity were scored semiquantitatively (grade 0–3) by gray-scale US (GSUS) and power Doppler US (PDUS). Patients with RA were examined at baseline and 3, 6, and 12 months after initiation of local or systemic therapy (disease-modifying antirheumatic drugs [DMARDs]/biologic agents). Erythrocyte sedimentation rate, anti–cyclic citrullinated peptide antibodies, and the clinical Disease Activity Score in 28 joints (DAS28) were determined.

Results

A cohort of 199 patients were analyzed and followed up over 12 months. At baseline, before modification of the therapy, patients received either DMARDs (n = 131), DMARDs plus biologic agents (n = 46), biologic monotherapy (n = 8), or no DMARD therapy (n = 14). At baseline, the mean DAS28 score was 4.6 and decreased to 3.2 after 1 year of therapy (P < 0.001). All US scores demonstrated a statistically significant improvement except for the PDUS scores for the shoulder and the hip. In detail, the mean synovitis GSUS score for the knee decreased from 5.2 at baseline to 2.2 after 12 months of followup. The mean GSUS score for the shoulder fell from 2.6 to 1.6, for the elbow fell from 5.2 to 2.6, and for the hip fell from 2.2 to 0.4 (P < 0.05 for each).

Conclusion

The SOLAR score is a feasible tool for the qualitative and quantitative evaluation of large joint involvement in patients with RA using US.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

Musculoskeletal ultrasound (US) is a valuable imaging tool in rheumatic diseases. It has been increasingly used in rheumatologic practice and research in the last decade, especially in small joints of the hands and fingers (1–3). By contrast, large joints have not been extensively studied, and knee involvement has only been incorporated in a 12-joint US score proposed by Naredo and colleagues (3). Evaluation of early soft tissue lesions and bony erosions in inflammatory joint disease is a strength of this method compared to conventional radiographs, which was demonstrated by Wakefield et al more than 10 years ago (2). In contrast to magnetic resonance imaging (MRI), there are almost no limiting factors, such as pacemakers, metal implants, or claustrophobia. Furthermore, US allows for a dynamic evaluation of inflamed joints, and is readily available.

Compared with clinical examination, gray-scale US (GSUS) is a more sensitive method for detecting synovitis and tenosynovitis. Therefore, several US scores have been introduced recently to estimate the inflammatory activity and the therapeutic response (3–6). The US scoring systems should facilitate therapeutic decisions and evaluate the efficacy of therapeutic interventions during longitudinal followup. These scores use a varying number of target joints examined by sonography. So far, mostly small joints such as the metacarpophalangeal (MCP), proximal interphalangeal (PIP), and metatarsophalangeal joints and wrists were included into the scanning protocols, being that these are the most affected joints in rheumatoid arthritis (RA).

However, large joints are also often involved in the arthritic process and represent a therapeutic challenge in daily rheumatologic practice. In the course of RA, the shoulder is, with regard to radiographic results, affected in up to 90% of patients, followed by the elbow in 60%, the knee in 30%, and the hip in 20% (7). In addition, large joint involvement represents an important prognostic factor associated with radiographic progression (8).

As demonstrated in small joints, GSUS and power Doppler US (PDUS) exhibit a higher sensitivity in detecting inflammation of large joints compared with clinical examination (9–12). Despite this, a US score for large joints has not yet been developed. Therefore, the main focus of this study was the establishment of a US score for large joint involvement in patients with RA suitable for daily rheumatologic practice. In addition, the sensitivity to change of this novel US score was assessed under certain therapies in patients with RA and concomitant arthritis of large joints.

Significance & Innovations

  • Ultrasound scoring in large joints has not been extensively studied.

  • A novel ultrasound scoring system has been developed to determine the degree of inflammation in large joints of patients with rheumatoid arthritis in a semiquantitative fashion.

  • This novel ultrasound score is a suitable tool for monitoring treatment responses in daily rheumatologic practice.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

Patients.

This national study started in April 2008 by founding a board of 6 rheumatologists with longstanding experience in musculoskeletal US (range 10–30 years, mean 18.5 years). First, relevant scanning planes for each joint were determined utilizing a Delphi procedure that took into consideration the rheumatologists' experience, the German and European League Against Rheumatism (EULAR) guidelines for musculoskeletal US, as well as published data (13–16). In a second step, a semiquantitative scoring system was developed for each joint region.

A total of 491 RA patients with an arthritic manifestation of at least 1 large joint were enrolled. A cohort of 199 of these patients with a diagnosis of RA had already undergone US examinations in 4 visits (baseline and after 3, 6, and 12 months) at 76 sites in Germany and were included in this analysis. The clinically most affected large joint (shoulder, elbow, hip, and knee) was chosen as the indicator joint in each individual patient and was sonographically evaluated after the initiation of therapy, or escalation of the established treatment (disease-modifying antirheumatic drugs [DMARDs] and/or biologic agents). In addition, several clinical as well as laboratory parameters were assessed.

Assessment.

At baseline and after 3, 6, and 12 months, 28 joints (bilateral shoulders, elbows, wrists, MCP joints, PIP joints, and knees) were clinically assessed for swelling and tenderness. The patient-rated visual analog scale for disease activity (range 0–100 mm) was also reported at each patient's visit. In addition, the following data were recorded on report sheets: year of birth, sex, height, weight, onset of typical symptoms, current rheumatologic therapy including DMARDs, biologic agents, and nonsteroidal antiinflammatory drugs, as well as systemic and intraarticular glucocorticoid dose at each visit.

The Disease Activity Score in 28 joints (DAS28) was used to assess disease activity at each visit.

Laboratory evaluation.

Erythrocyte sedimentation rate (ESR; normal level <20 mm/hour) was obtained at each visit. IgM rheumatoid factor (RF; normal level <24 IU/ml) and anti–cyclic citrullinated peptide (anti-CCP) antibodies (normal level <20 units/ml) were determined at baseline.

US examination.

The most affected large joint (shoulder, elbow, hip, and knee) was sonographically examined in a standardized modified manner according to the German (13–16) and EULAR (17) guidelines at the baseline and the followup visits. The determined joint regions were assessed by GSUS and PDUS.

GSUS.

Synovitis by GSUS was analyzed semiquantitatively from 0–3 (0 = absent, 1 = mild, 2 = moderate, and 3 = severe) (Table 1). Grade 1 represented a small hypoechoic/anechoic line beneath the joint capsule. For grade 2, the joint capsule had to be elevated parallel to the joint area. Grade 3 was characterized by a strong convex distension of the joint (Table 1). Tenosynovitis and erosions were registered as being absent (0) or present (1). Erosions were defined as an interruption of the bone surface in 2 perpendicular planes. Tenosynovitis represented a hypoechoic or anechoic thickened tissue with or without fluid within the tendon sheath.

Table 1. Grading of synovitis by gray-scale ultrasound*
Region and planeGrade 0Grade 1Grade 2Grade 3
  • *

    JCD = joint capsule distension.

Shoulder    
 Posterior transverseNormalEffusion/synovitis with maximal external rotation onlyEffusion/synovitis in external and internal rotationRemarkable convex JCD
 Axillary longitudinalNormalJCD concaveJCD straightJCD convex
Elbow    
 HumeroradialNormalJCD parallel to the capitulum humeriJCD straightJCD convex
 HumeroulnarNormalJCD parallel to the trochlea humeriJCD straightJCD convex
 Olecranon fossaNormalOlecranon fossa partially filledOlecranon fossa completely filledJCD convex above the olecranon fossae
Hip    
 Anterior longitudinalNormalJCD concave to femur neckJCD straightJCD convex
Knee    
 Suprapatellar longitudinalNormalJCD parallel to femur boneJCD straightJCD convex
 Medial/lateral longitudinal of femorotibial jointNormalJCD parallel to bone, no distension over the joint spaceJCD parallel to bone, distension above the joint spaceJCD convex above the joint space
Dorsal longitudinal scanNormalSlight JCD over the joint spaceJCD parallel to bone, distension over the joint spaceJCD convex above the joint space

GSUS for the different joints was performed as follows: The shoulder joint was evaluated in the posterior transverse scan and the axillary longitudinal scan for synovitis and/or effusion. Only these 2 planes were judged suitable for scoring (Table 1). The subdeltoid bursa and the long biceps tendon were examined in the anterior transverse scan only for presence of effusion and tenosynovitis, but did not influence the score. Four planes were analyzed for the detection of erosions: the ventral transverse scan, the dorsal transverse scan, the axillary longitudinal scan, and the lateral longitudinal scan.

The elbow joint was examined in the humeroradial as well as the humeroulnar longitudinal scan, and the dorsal longitudinal scan above the olecranon fossa (Table 1). To score the degree of synovitis of the hip joint, the anterior longitudinal scan was analyzed (Table 1). The knee joint was divided into 4 planes to score for synovitis: the suprapatellar longitudinal scan (Figure 1), the medial longitudinal scan, the lateral longitudinal scan, and the dorsal longitudinal scan. (Table 1).

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Figure 1. Synovitis scored by gray-scale ultrasound. Knee, suprapatellar longitudinal plane: A, grade 0, B, grade 1, C, grade 2, and D, grade 3.

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PDUS.

PDUS was performed for synovitis and tenosynovitis in each scanning plane described above. The semiquantitative findings of PDUS activity for synovitis were scored as follows: grade 0 = no intraarticular color signal, grade 1 = up to 3 single color signals or 2 single color signals and 1 confluent color signal representing only low flow, grade 2 = grade >1 to <50% of the intraarticular area filled with color signals representing clear flow, and grade 3 = >50% of the intraarticular area filled with color signals (5) (Figure 2).

thumbnail image

Figure 2. Lateral longitudinal view of the knee. Synovitis scored by power Doppler ultrasound. A, grade 0, B, grade 1, C, grade 2, and D, grade 3.

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Based on these results, a score for each large joint (shoulder, elbow, hip, and knee) was developed, including the sum of the synovitis scores in the GSUS and the PDUS modes. Depending on the number of scored planes per joint, the score values were different for the shoulder (GSUS/PDUS 0–6), the elbow (GSUS/PDUS 0–9), the hip (GSUS/PDUS 0–3), and the knee (GSUS/PDUS 0–12).

US interreader and intrareader reliability.

Twenty-four readers took part in the US reliability substudy. The reading of a specialist in musculoskeletal US (WH) was used as the imaging gold standard. Sixty stored images (22 for the elbow, 20 for the knee, 11 for the shoulder, and 7 for the hip) were scored for synovitis in GSUS and synovitis in PDUS using blinded conditions. Analysis was performed semiquantitatively (grade 0–3) for synovitis in GSUS and PDUS. For intrareader testing, 6 US images were evaluated twice.

Statistical analysis.

Statistical analysis was performed with SPSS statistical software, version 17.02. For quantitative parameters (e.g., the number of patients, age of the examined patients, and their disease activity), the mean ± SD and range were determined for each. Significant changes were calculated by the Kruskal-Wallis test. P values less than 0.05 were considered statistically significant.

Interreader and intrareader agreement were calculated using kappa coefficients between the readers. The kappa coefficients were divided as follows: <0.0 = poor, 0–0.20 = slight, 0.21–0.40 = fair, 0.41–0.60 = moderate, 0.61–0.80 = substantial, and 0.81–1.0 = almost perfect agreement (18). Percentage agreements were also calculated.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

Patient characteristics.

A cohort of 199 patients (67% women) with a mean ± SD age of 53.6 ± 14.4 years were examined at 4 visits (baseline and after 3, 6, and 12 months). All patients had RA according to the 1987 American College of Rheumatology criteria (19). At inclusion, 58% of the patients were RF positive and 52% of the patients had tested positive for anti-CCP antibodies.

Medication.

A total of 78% of the patients received steroids (55% systemic administration, 15% systemic and local intraarticular administration, and 8% local intraarticular injections into the target joint only).

At baseline patients were treated with either DMARDs (n = 131 [70%]), a combination of DMARDs plus biologic agents (n = 46 [24%]), or biologic monotherapy (n = 8 [4%]). Fourteen patients had no DMARD or biologic therapy at the time of enrollment. The following DMARDs were administered: methotrexate (n = 115), leflunomide (n = 37), sulfasalazine (n = 12), chloroquine/hydroxychloroquine (n = 4), azathioprine (n = 2), and cyclosporine (n = 1). In addition, the following biologic agents were administered: 35 (64%) of these patients received adalimumab, 11 patients (20%) received etanercept, 3 patients (5%) received tocilizumab, 2 patients (4%) received golimumab, 1 patient (2%) received infliximab, 1 patient (2%) received rituximab, and 1 patient (2%) received abatacept.

During the 12-month observation period, the immunosuppressive treatment had been adjusted individually for each patient with RA based on the clinical findings and the experience of the treating rheumatologist.

US, clinical, and laboratory parameters.

US, clinical, and laboratory results for the entire group are shown in Table 2. The mean synovitis score for GSUS for the knee (n = 132) was 5.2 at baseline and decreased significantly to 2.2 (P < 0.001) after 12 months of followup. The mean PDUS score was calculated as 4.0 before changing the treatment and decreased to 1.3 within the following 12 months (P < 0.001). For the shoulder (n = 46), the mean GSUS score decreased from 2.6 to 1.6 (P < 0.07), and the mean PDUS score decreased from 1.5 to 0.7 (P < 0.09). For the elbow (n = 42), the mean GSUS score fell from 5.2 at baseline to 2.6 (P < 0.001) 12 months after initiation of a new therapy regimen, and the mean PDUS score decreased from 2.4 to 0.9 (P < 0.003). For the hip (n = 15), a decline of the mean GSUS score from 2.2 to 0.4 (P < 0.001) was observed, and for the mean PDUS score from 1.5 to 0.1 (P < 0.06).

Table 2. US, clinical, and laboratory data (n = 199)*
Joint regionBaseline3 months6 months12 months
  • *

    Values are the mean ± SD. US = ultrasound; GSUS = gray-scale US; PDUS = power Doppler US; DAS28 = Disease Activity Score in 28 joints; ESR = erythrocyte sedimentation rate.

  • P < 0.001 (2-sided significance by Kruskal-Wallis test).

  • ‡, †

    P < 0.05 (2-sided significance by Kruskal-Wallis test).

Shoulder (n = 46, score range 0–6)    
 GSUS2.6 ± 1.92.0 ± 1.61.8 ± 1.51.6 ± 1.7
 PDUS1.5 ± 1.61.0 ± 1.51.1 ± 1.50.7 ± 1.3
Elbow (n = 42, score range 0–9)    
 GSUS5.2 ± 2.33.6 ± 2.93.2 ± 2.92.6 ± 2.9
 PDUS2.4 ± 2.11.6 ± 2.01.3 ± 1.70.9 ± 1.2
Hip (n = 15, score range 0–3)    
 GSUS2.2 ± 0.61.3 ± 1.00.7 ± 0.70.4 ± 0.7
 PDUS1.5 ± 1.20.4 ± 0.50.3 ± 0.50.1 ± 1.2
Knee (n = 132, score range 0–12)    
 GSUS5.2 ± 2.93.1 ± 2.72.9 ± 2.72.2 ± 2.6
 PDUS4.0 ± 3.12.4 ± 2.71.9 ± 2.41.3 ± 2.1
DAS28 score4.6 ± 1.33.6 ± 1.43.5 ± 1.33.2 ± 1.3
ESR, mm/hour31.5 ± 22.523.9 ± 18.721.7 ± 16.920.9 ± 16.9

In line with the observed improvement of the Sonography of Large Joints in Rheumatology (SOLAR) scores, a significant reduction of the mean DAS28 score was determined, changing from a baseline value of 4.6 to 3.2 (P < 0.001) at 12 months of followup. There was a significant reduction of the mean ESR within the same period, which dropped from 31.5 mm/hour to 20.9 mm/hour reflecting treatment response.

Unfortunately, the data set for the erosion scores including the followup was incomplete and did not provide sufficient power to allow for statistical analysis.

Interreader and intrareader reliability of the US assessment.

For the semiquantitative scoring (0–3) of the stored images for synovitis in GSUS and PDUS, the overall kappa values were 0.45 (mean interreader agreement 62%) for GSUS and 0.59 (mean interreader agreement 75%) for PDUS.

The following results for intrareader reliability were observed: the mean kappa values for semiquantitative scoring for GSUS were 0.59 (mean intrareader agreement 83%) for the shoulder and 0.79 (mean intrareader agreement 74%) for the hip. In addition, the kappa values for PDUS were 0.65 (mean intrareader agreement 97%) for the shoulder and 0.7 (intrareader agreement 83%) for the knee.

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

Musculoskeletal US is a well-established imaging method that is routinely used in daily practice by numerous rheumatologists for both evaluating disease activity and monitoring therapy. In recent years, several US scores have been developed to evaluate and quantitate the overall inflammatory activity in patients with RA and psoriatic arthritis (3, 5). These scores mainly focus on small joints, reflecting the predominant affection of these joints in RA. However, daily experience demonstrates that large joints are frequently involved in rheumatic diseases, and that involvement of large joints has an enormous impact on the patient's disability and prognosis (20).

Hermann et al reported on shoulder involvement in up to 70% of patients with RA confirmed by MRI scanning (21). In addition, erosions of the elbow joint have been observed in 61% of patients with RA followed up for 15 years (22), whereas hip erosions were detected in 20% of patients with RA, and erosive changes of the knees were detected in 27% of patients with RA within a period of 12 years (7). Sonographically evident hip synovitis has been observed in 22% of patients with active RA (23). In a recently published sonographic study, synovial hypertrophy in the knee joint was detected by GSUS in 82% of patients with RA and, in 19% of patients, hypervascularity was detected in the knee by PDUS (24).

With regard to these results, and considering the low sensitivity of clinical assessment concerning inflammatory changes in large joints (9–12), we initiated a US scoring system for the shoulder, elbow, hip, and knee joint separately. Since US is a potentially time-consuming imaging modality, evaluation of the feasibility and practicability of the new scoring system was a major aspect. Therefore, 2 standardized scanning planes were defined for the shoulder joint (the posterior transverse scan and the axillary longitudinal scan). According to published data and our own experience, these scanning planes allow for detection of up to 95% of effusions/synovitis in the glenohumeral joint (12, 25, 26). Furthermore, scans of these 2 planes can be performed easily and are quickly applied. In line with these considerations, 87% of the glenohumeral synovitis was detected in the axillary and 90% in the dorsal transverse scan (25), whereas 94% of the glenohumeral effusions were observed in the dorsal transverse scan following maximal external rotation.

The scanning protocol for the elbow covers the anterior humeroradial, the anterior humeroulnar, and the posterior longitudinal scan over the olecranon fossa facilitating the delineation of the joint capsule and pathologic distensions. These planes have been successfully utilized for detection of effusion and synovitis in the elbow joint (27).

The anterior longitudinal scan was chosen to be the best for the scoring of synovitis and hypervascularisation in the hip as previously proposed by Boutry et al (28). In addition, a high correlation between histopathologically confirmed vascularity and PDUS signal activity has been demonstrated for the anterior longitudinal scan (29).

The knee was scanned in GSUS in 4 standardized planes: the suprapatellar longitudinal, the medial longitudinal, the lateral longitudinal, and the dorsal longitudinal scan. The infrapatellar longitudinal scan was additionally added to the PDUS score, whereas only the suprapatellar longitudinal scan and the medial and lateral recessus have been analyzed in previous studies to estimate the inflammatory activity.

Previously, the synovial thickness and power Doppler flow have been measured in the suprapatellar and parapatellar pouch (30), whereas the knee has been scanned in the suprapatellar and parapatellar planes by other investigators (31). In addition, synovitis of the knee has been scored in the suprapatellar longitudinal and transversal plane, and the diameter of the power Doppler signal and the resistance index have been determined (32).

According to our experience, the suprapatellar and especially the medial and lateral longitudinal scans are the most suitable to detect hypervascularization of an inflamed knee joint; therefore, these planes have been included in the novel scanning protocol.

Utilizing the novel SOLAR score for longitudinal followup of our cohort, a significant reduction has been observed in the GSUS and PDUS scores for the elbow and the knee within 6 and 12 months following treatment adjustment. In addition, GSUS demonstrated significant improvement of scores for the shoulder and the hip joints. PDUS scores for the shoulder and the hip also improved, but this did not reach a statistically significant level due to the relatively small number of examined joints. Corresponding to the US scores, the beneficial treatment response was also reflected by a highly significant reduction of DAS28 scores at 3, 6, and 12 months following initiation or modification of the antirheumatic treatment.

One major limitation of this study is the lack of a gold standard to adjust the US grading. In particular, MRI scores have only been established for small joints, and therefore this technique could not be implemented to validate the novel SOLAR score (33). In addition, established scoring systems for conventional radiographs of large joints do not account for soft tissue alterations and therefore could not be utilized for validation of the SOLAR score either (34).

Mixing signs of inflammatory activity (synovitis) with structural lesions (erosions) in the same scoring system could be considered problematic. However, US is able to detect structural damage earlier than radiographs, which is similar to MRI. Therefore, we decided to add the presence of erosions as clinically important information to the novel scoring system assuming that erosive disease should be treated more aggressively. In line with this, both synovitis as well as erosions have been included together as substantial aspects in established US (German US7 score) and MRI (Rheumatoid Arthritis MRI Scoring System) scores.

Furthermore, one could object that only the clinically most affected large joint is followed up by US, and this would introduce a selection bias. However, there is only a small likelihood to detect relevant pathologic findings by US in clinically unaffected joints, which is of course not precluded. However, one might envisage a new study to determine the involvement of clinically unaffected large joints in patients with RA utilizing the newly developed US score.

Another limitation of this study might be the fact that patients were examined by numerous observers with different US equipment. Although US is considered to be a strongly observer-dependent modality, several studies demonstrate a moderate to good interreader agreement supporting utilization of this method to assess joint involvement in patients with RA (35, 36).

In order to verify interreader and intrareader agreement of the SOLAR score, a reliability study has been performed additionally. The results of this study partly revealed moderate to good kappa values demonstrating the feasibility to apply the SOLAR score for improved clinical assessment.

In conclusion, the SOLAR score is a valuable tool for the quantitative and qualitative evaluation of large joint involvement in patients with RA using US. In addition, the SOLAR score is suitable for monitoring treatment responses in daily practice.

AUTHOR CONTRIBUTIONS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be published. Dr. Hartung had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study conception and design. Hartung, Kellner, Strunk, Backhaus.

Acquisition of data. Hartung, Kellner, Strunk, Sattler, Schmidt, Backhaus.

Analysis and interpretation of data. Hartung, Ehrenstein, Fleck, Backhaus.

ROLE OF THE STUDY SPONSOR

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

Abbott GmbH & Company KG, Germany, an affiliate of Abbott Laboratories, supported the logistic procedure of the ultrasound project. They agreed to the submission of the manuscript for publication and approved the manuscript, but did not have any influence on the study design, data collection, data analysis, or writing of the manuscript.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES

We thank Mrs. Imma Fischer, PhD, Department of Biostatistics, Tübingen, Germany, and the US and clinical research investigators involved in this study.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. AUTHOR CONTRIBUTIONS
  8. ROLE OF THE STUDY SPONSOR
  9. Acknowledgements
  10. REFERENCES
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