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Breast Imaging |
1 From the Departments of Radiology (M.M., C.C.R., A.K., W.M., T.H.H.), Gynecology (A.G.), and Pathology (M.R.), Medical University Vienna, General Hospital of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria. From the 2003 RSNA Annual Meeting. Received April 26, 2005; revision requested June 22; revision received August 9; accepted September 7; final version accepted February 1, 2006. Address correspondence to M.M. (e-mail: mazda.memarsadeghi{at}meduniwien.ac.at).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Materials and Methods: The study was approved by the university ethics committee; written informed consent was obtained. Twenty-two women (mean age, 60 years; range, 40–79 years) with breast carcinomas underwent nonenhanced and USPIO-enhanced (2.6 mg of iron per kilogram of body weight intravenously administered) transverse T1-weighted and transverse and sagittal T2-weighted and T2*-weighted MR imaging in adducted and elevated arm positions. Two experienced radiologists, blinded to the histopathologic findings, analyzed images of axillary lymph nodes with regard to size, morphologic features, and USPIO uptake. A third independent radiologist served as a tiebreaker if consensus between two readers could not be reached. Visual and quantitative analyses of MR images were performed. Sensitivity, specificity, and accuracy values were calculated. To assess the effect of USPIO after administration, signal-to-noise ratio (SNR) changes were statistically analyzed with repeated-measurements analysis of variance (mixed model) for MR sequences.
Results: At nonenhanced MR imaging, of 133 lymph nodes, six were rated as true-positive, 99 as true-negative, 23 as false-positive, and five as false-negative. At USPIO-enhanced MR imaging, 11 lymph nodes were rated as true-positive, 120 as true-negative, two as false-positive, and none as false-negative. In two metastatic lymph nodes in two patients with more than one metastatic lymph node, a consensus was not reached. USPIO-enhanced MR imaging revealed a node-by-node sensitivity, specificity, and accuracy of 100%, 98%, and 98%, respectively. At USPIO-enhanced MR imaging, no metastatic lymph nodes were missed on a patient-by-patient basis. Significant interactions indicating differences in the decrease of SNR values for metastatic and nonmetastatic lymph nodes were found for all sequences (P < .001 to P = .022).
Conclusion: USPIO-enhanced MR imaging appears valuable for assessment of axillary lymph node metastases in patients with breast carcinomas and is superior to nonenhanced MR imaging.
© RSNA, 2006
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Different imaging techniques—magnetic resonance (MR) imaging, computed tomography (CT), and ultrasonography (US)—allow visualization of lymph nodes that may not be palpable at physical examination (14–25). With these imaging techniques, the preoperative assessment of axillary lymph node metastases is based mainly on measurement of nodal dimensions, such as maximum transverse diameter (18–23) or ratios of maximum longitudinal to maximum transverse diameter (24), and, therefore, these techniques are somewhat limited. In addition, morphologic criteria (eg, shape, thickened lobular cortex, displacement and/or absence of fatty hilus), enhancement patterns, and grouping of lymph nodes are further important parameters (15–26). All these criteria remain controversial, and recommendations for differentiation between nonmetastatic and metastatic lymph nodes vary widely (5,11,15–26).
A lymph node–specific MR contrast agent has been developed that allows the identification of malignant nodal infiltration independent of lymph node size. This MR contrast agent is classified as a nanoparticle (mean diameter, 30 nm) and is composed of an iron oxide core coated with low-molecular-weight dextran. The class of these MR contrast agents is collectively known as ultrasmall superparamagnetic iron oxide (USPIO). After intravenous USPIO administration, nonmetastatic lymph nodes generally show uptake of contrast material, which results in decreased signal intensity (SI) on T2- and T2*-weighted MR images, whereas metastatic lymph nodes generally do not exhibit any uptake, and SI remains unchanged (26–38). This stability in SI within metastatic lymph nodes has been attributed to replacement of macrophages by metastatic cells, which lack reticuloendothelial activity and show no USPIO uptake (4,5,26,27,31–38). Findings in studies of patients with head and neck, urologic, pelvic, rectal, and breast cancers have confirmed the potential for improved detection of lymph node metastases with USPIO-enhanced MR imaging when compared with detection with nonenhanced or gadolinium-enhanced MR imaging (4,5,32–38).
USPIO-enhanced MR imaging in patients with breast cancer has been reported infrequently (4,5). Thus, the purpose of our study was to prospectively assess the accuracy of nonenhanced versus USPIO-enhanced MR imaging for the depiction of axillary lymph node metastases in patients with breast carcinoma by using histopathologic findings as the reference standard.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Patients
In a 5-month period, 25 consecutive female (three premenopausal and 22 postmenopausal) patients (mean age, 62 years; range, 40–85 years) who met our inclusion criteria were enrolled in this prospective phase III clinical trial (trial no. G-534-70). Of the 25 patients, three patients were excluded. In two of these three patients, surgery was performed without axillary lymph node dissection; in the third patient, who was initially scheduled for surgery, preoperative chemotherapy was administered as a result of the clinical findings of the preoperative staging. For final statistical analysis, we included 22 consecutive female (three premenopausal and 19 postmenopausal) patients (mean age, 60 years; range, 40–79 years). The study was approved by the ethics committee of our university; written informed consent was obtained from all patients.
Inclusion and Exclusion Criteria
The inclusion criteria were as follows: (a) patients with breast carcinoma confirmed histopathologically by using percutaneous image-guided core breast biopsy at presentation (39), (b) patients scheduled to undergo surgery with lymphadenectomy within 15 days after USPIO-enhanced MR imaging, and (c) patients with at least one lymph node that could be potentially compared with one lymph node that was available for histopathologic analysis at presentation.
The exclusion criteria were as follows: (a) patients with a contraindication to MR imaging; (b) patients with a known allergy to dextran or drugs containing iron salts; (c) patients who underwent chemotherapy and/or radiation therapy; (d) patients in whom no lymphadenectomy was performed; (e) pregnant or breastfeeding patients; (f) patients whose degree of cooperation was incompatible with performance of the study; (g) patients participating in another clinical trial, including that of an investigational drug; and (h) patients in the care of a guardian.
Contrast Agent
The USPIO contrast agent (Combidex, Advanced Magnetics; Sinerem, Guerbet) was provided as a lyophilized powder consisting of ultrasmall biodegradable superparamagnetic particles with a total particle diameter in solution of 17–21 nm. USPIO particles coated with low-molecular-weight dextran were reconstituted with 10 mL of sterile 0.9% normal saline and yielded a dark reddish brown aqueous solution containing 26 mg of USPIO per milliliter. The contrast agent (2.6 mg of iron per kilogram of body weight) was administered intravenously in a single dose with drip infusion through an infusion filter (0.22-µm pore size) after it was diluted in 100 mL of saline at a rate of 4 mL/min.
Imaging Technique
MR imaging was performed with a 1.0-T imaging unit (Gyroscan T10-NT; Philips Medical Systems, Best, the Netherlands) immediately before and after the administration of USPIO. USPIO-enhanced MR imaging was performed within 24–36 hours after the end of the contrast material uptake, and the end of uptake was based on a maximum iron peak level in lymph nodes between 1 and 3 days after injection (28). All examinations were performed by using a dedicated large, flexible surface body coil (Synergy; Philips Medical Systems), which was wrapped around the axillary regions in the adducted and elevated arm positions, with the patient in the supine position.
After a localizer image of the axilla was obtained, the following sequences, before and after the USPIO application, were performed: T1-weighted three-dimensional (3D) fast field echo (FFE) (repetition time msec/echo time msec, 24/7; section thickness, 3 mm; matrix, 256 x 256; flip angle, 30°; one signal acquired), T2*-weighted FFE (683/14; section thickness, 4 mm; matrix, 256 x 512; flip angle, 20°; two signals acquired; gap, 0.4 mm), and T2-weighted fast spin echo (SE) (7600/120; section thickness, 4 mm; matrix, 256 x 256; three signals acquired; gap, 0.4 mm; echo train length, 11). For the T1-weighted 3D FFE and the T2*-weighted FFE sequences, a field of view of 18 x 18 cm was used, and for T2-weighted fast SE sequences, a field of view of 25.6 x 25.6 cm was used.
The T1-weighted 3D FFE sequences were performed in the transverse plane. The T2*-weighted FFE and T2-weighted fast SE sequences were performed in the transverse and sagittal planes. Imaging was performed in the transverse planes with the arm in both adducted and elevated positions for all sequences. Imaging was performed in the sagittal plane only with the arm in the elevated position. MR examination of the axilla could be performed in all 22 patients. Total acquisition time for all sequences per session was less than 40 minutes.
All 22 patients tolerated the administration of the USPIO contrast agent well without any discomfort or adverse reaction.
Evaluation.—A combined evaluation of nonenhanced and USPIO-enhanced MR images was completed prior to surgery and before the pathologic results were known. To assess the interobserver agreement rate, two radiologists (M.M., A.K., with 5 and 3 years of experience in breast MR imaging, respectively) independently reviewed the studies from hard-copy films. For cases for which 100% agreement was not achieved with independent reading, a consensus reading was reached after group discussion between two readers. A third independent reader (T.H.H.) with more than 12 years of experience in breast MR imaging, who was blinded to the results of analysis of the two first readers and provided subjective interpretation of lymph nodes, served as a tiebreaker if consensus between the two readers could not be reached. Each radiologist reviewed MR imaging studies without conventional studies such as mammography and US. Although the readers knew the patients had proved breast cancer, they were blinded to the clinical findings, initial reports (including size of the lesions), and histopathologic diagnosis from analysis of axillary lymph nodes. The criteria used to distinguish nonmetastatic from metastatic nodes included size and USPIO uptake. Although lymph node detection was easiest on T2-weighted fast SE images, lymph node size was measured on T1-weighted 3D FFE images to minimize interference with susceptibility effects and, thus, overestimation of size.
On the nonenhanced MR images, lymph nodes were rated as metastatic on the basis of nodal size and shape criteria as described by Michel et al (5). A short-axis diameter exceeding 10 mm was considered indicative of a metastatic node, as was a round rather than an oval shape. The distinction between round and oval nodes was made on the basis of the ratio between the long axis and the short axis. A node was called round if this ratio was smaller than 1.5. A node was called oval if this ratio was larger than 1.5 (5,40,41). The short-axis diameter was measured by using the metric standardized scale included on each image.
For the USPIO-enhanced MR images, visual analysis was based on the following criteria: Nonenhanced and USPIO-enhanced T2*-weighted FFE and T2-weighted fast SE images were compared. Lymph nodes with a homogeneous SI decrease on USPIO-enhanced images, compared with the SI on nonenhanced images, were considered nonmetastatic lymph nodes. Lymph nodes with no SI decrease or uniformly high SI on USPIO-enhanced images, compared with the SI on nonenhanced images, were considered metastatic lymph nodes. Lymph nodes also were considered metastatic if a partial SI decrease could be observed. A partial SI decrease included (a) nodes with a central area of hyperintensity (excluding a fatty hilum) but a peripheral decrease in SI, (b) discrete focal defects (isolated islands of high SI), or (c) nodes with a central area of hypointensity but without a peripheral SI decrease (35) (Fig 1).
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Every lymph node with a diagnosis was drawn on the map, and the number and localization were indicated according to the described levels. Results of MR imaging analysis of the axillary lymph nodes (number, size, and anatomic level of metastatic nodes) were reported to the referring surgeon prior to surgery, and an outline of the lymph nodes was drawn and made available to the surgeon and pathologist prior to surgery. The map of the axilla and MR images were discussed with surgeons and pathologists. In cases of discrepant numbers of lymph nodes counted at MR imaging and histopathologic analysis, the smaller number of detected nodes was defined as the total number in each patient.
Quantitative image analysis.—Lymph node SI was evaluated on the nonenhanced and USPIO-enhanced MR images obtained with all sequences by using a region of interest evaluation in relation to the background noise. The SI of the background noise was measured in the air outside the patient. The size of the region of interest for the background noise was fixed to 2 cm in diameter. Operator-defined region of interest SI measurements were taken directly from the monitor (Easy Vision 4.2; Philips Medical Systems) for each lymph node. The size of the region of interest was adjusted to the size of the lymph node between 3 mm and 3.3 cm. For lymph nodes with partial contrast agent uptake, the region of interest included the area with partial contrast agent uptake. In each patient, the SI measurement was performed for all metastatic lymph nodes and for at least three nonmetastatic lymph nodes for comparison. The signal-to-noise ratio (SNR) for each lymph node was calculated by using the following equation: SNR = SIlymn/SDair, where SIlymn is SI of the lymph node and SDair is standard deviation of air. Because USPIO has predominantly T2 and T2* shortening effects, the low SNR represents the decreased SI of lymph nodes, which is expected with nonmetastatic nodes, whereas a high SNR represents metastatic nodes. A lymph node was considered metastatic if a decrease in SNR of less than 30% was present on the USPIO-enhanced T2*-weighted FFE or T2-weighted fast SE images (35).
Surgery and Histopathologic Evaluation
More than one surgeon (A.G.) with at least 5 years of experience in breast surgery performed surgery within 2 weeks after MR imaging (range, 1–13 days). All patients underwent breast-sparing surgery. Tumors were located in the left breast in 12 patients and in the right breast in 10 patients. A tumor stage pT1 (size, 
20 mm in greatest dimension) was diagnosed in 13 patients, and a tumor stage pT2 (size, >20 mm but 50 mm) was diagnosed in nine patients. Axillary dissection was performed in 22 patients by using a block resection of levels 1 and 2 of the ipsilateral side, regardless of MR imaging findings. Acquired information from the sampled lymph nodes, according to levels and anatomic regions, was provided to the pathologist by the surgeon. An experienced breast pathologist (M.R.) with 20 years of experience in breast disease analyzed resected specimens histopathologically. A lymph node was regarded as metastatic when tumor cells were present at light microscopy.
For the final evaluation on a node-by-node basis, only those lymph nodes were included that could be unequivocally identified with all MR imaging sequences, before and after USPIO administration, and for which an unambiguous match with histopathologic findings was feasible. Thus, a correlation between results of MR imaging and histopathologic findings was feasible for 133 lymph nodes.
Statistical Analysis
Data were analyzed by using statistical software (SPSS, release 11.5; SPSS, Chicago, Ill) and confidence interval analysis (CIA, release 2.1.2, 2000; Trevor Bryant, University of Southampton, Southampton, England). Results are expressed as the mean ± standard deviation. Sensitivity, specificity, and accuracy values were calculated for nonenhanced and USPIO-enhanced MR imaging on node-by-node and patient-by-patient bases. Taking multiple measures per patient into account, we used a mixed model to compare the short-axis diameter of metastatic and nonmetastatic lymph nodes. Weighted two-way analysis of variance with repeated measures (mixed model) was used to compare the per-patient mean values of the SNR measurements for nonmetastatic and metastatic lymph nodes at nonenhanced and USPIO-enhanced MR imaging for each sequence, as well as the interactions between mean values of the SNR measurements for nonmetastatic and metastatic lymph nodes at nonenhanced and USPIO-enhanced MR imaging for each sequence (42). The weight factor was included to account for differences across patients in the numbers of metastatic and nonmetastatic lesions. All P values obtained for multiple testing were corrected by using the Bonferroni-Holm procedure. A corrected P value of less than .05 was considered to indicate a significant difference. To assess the interobserver agreement, 
coefficients were calculated. Sensitivity, specificity, and accuracy in the node-by-node evaluation were calculated with the assumption of independency of diagnoses of lymph nodes and by using the weighted means of the characteristic values stratified for every person to consider repeated measurements. Statistical analysis was performed by using histopathologic findings as the reference standard.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Five lymph nodes were characterized as false-negative, 23 as false-positive, six as true-positive, and 99 as true-negative (Table 1). At first, statistical evaluation was based on the assumption that diagnoses of lymph nodes are independent if they are obtained from the same patient. On the basis of this assumption, the node-by-node evaluation revealed a sensitivity of 55%, a specificity of 81%, and an accuracy of 79%. When we considered repeated measurements by using the weighted means of characteristic values stratified for each person, sensitivity changed to 71%, specificity to 84%, and accuracy to 79% in the node-by-node evaluation. In the patient-by-patient evaluation, 11 patients were characterized as having a false-positive finding, and in one patient, a metastatic lymph node was missed. Statistical evaluation of nonenhanced MR imaging revealed a sensitivity of 83%, a specificity of 31%, and an accuracy of 45% in the patient-by-patient evaluation.
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Eleven lymph nodes were rated as true-positive, and 120 were rated as true-negative. Two lymph nodes were rated as false-positive. No false-negative lymph nodes were found. At first, statistical evaluation was based on the assumption that diagnoses of lymph nodes are independent even if they are obtained from the same patient. On the basis of this assumption, the node-by-node evaluation revealed a sensitivity of 100%, a specificity of 98%, and an accuracy of 98% (Table 2). When we considered repeated measurements by using the weighted means of characteristic values stratified for each person, sensitivity was 100%, and specificity changed slightly to 98.07% and accuracy to 98.04% in the node-by-node evaluation. In the patient-by-patient evaluation at USPIO-enhanced MR imaging, no false-positive or false-negative case was reported. Statistical evaluation revealed, for USPIO-enhanced MR imaging, that sensitivity, specificity, and accuracy were 100% in the patient-by-patient evaluation.
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= 0.915), as well as the patient-by-patient, evaluation ( = 1.000) at USPIO-enhanced MR imaging. A disagreement occurred in two (2%) of 133 metastatic lymph nodes in two patients with more than one metastatic lymph node. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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In accordance with findings in previous studies (4,5,14,19–22,34–38), we found size to be an unreliable criterion at nonenhanced MR imaging due to overlap of the short-axis diameter of nonmetastatic and metastatic lymph nodes. In our evaluation, nonenhanced MR imaging revealed a sensitivity of 55%, a specificity of 81%, and an accuracy of 79%.
With regard to axillary lymph node staging, there are few published data for USPIO-enhanced MR imaging (4,5). Stets and co-workers (4) evaluated different diagnostic and technical parameters in their study and did not focus on a patient-by-patient evaluation. Michel and co-workers (5) assessed the value of MR imaging after USPIO application only and did not include nonenhanced MR imaging in their evaluation. Researchers in both studies reported a sensitivity of 80%–90% and a specificity of 90%–100% in the node-by-node evaluation. Our results from the node-by-node evaluation are in keeping with those in these reports; however, we attained a higher level of sensitivity, specificity, and accuracy.
These higher levels may be attributable to several reasons: First, we used a section thickness of 3 or 4 mm. Thus, nodes that were 3 mm or larger could be confidently identified in the transverse plane. Second, use of a 256 x 256 matrix and a small field of view (185 mm) enabled achievement of an in-plane resolution of approximately 0.7 x 0.7 mm, although micrometastases of 1 mm or smaller would still be difficult or impossible to detect at this resolution. The use of now available high-spatial-resolution T2-weighted sequences and high-field-strength MR units (>3 T), however, may further improve the detection of infiltration of small metastatic lymph nodes, as demonstrated by Heesakkers et al (43). Finally, we examined the axilla in different orientations, which helped us to discriminate better the relationship between the lymph nodes and adjunct vessels and allowed a more detailed analysis of the lymph nodes.
In addition to the node-by-node evaluation, we performed a patient-by-patient evaluation, which resulted in an almost perfect accuracy rate for this technique compared with the results reported in the literature. These results rely on the same technical improvements as described for the node-by-node evaluation. Another reason for these results, however, is the simpler approach in the evaluation of the axillary lymph nodes: In the patient-by-patient evaluation, the detection of one lymph node metastasis is sufficient to predict a case as positive.
Another technique is sentinel lymph node imaging, which is an accepted alternative to radical axillary lymph node dissection in patients with breast cancer (6,13,44). Thus, compared with the sentinel lymph node technique, the patient-by-patient approach in USPIO-enhanced MR imaging of the axilla has the potential to be used as a noninvasive and nonionizing method in the evaluation of lymph node metastases.
As suggested by Mack et al (36), we found different enhancement patterns in metastatic and nonmetastatic lymph nodes after USPIO administration, with no quantitative overlap. In accordance with Koh et al (37), we found T2-weighted MR imaging to be superior to T2*-weighted MR imaging for the identification of nodes within the axilla, because nodes were readily distinguished from blood vessels. Conversely, the T2*-weighted FFE sequence, which is more sensitive to the susceptibility effects of iron, was more successful for characterization of the uptake of USPIO into nodes. The T2*-weighted FFE sequence employs signal averaging from five echo times and, thus, allows reduction of movement and chemical shift artifacts (26). On the other hand, because both lymph nodes and vessels were similarly high in SI on T2*-weighted images before administration of USPIO, they may be mistaken for one another. Thus, we suggest that both T2- and T2*-weighted imaging should be performed for the assessment of axillary lymph nodes. Although nonenhanced T1-weighted MR imaging is not considered a state-of-the-art technique for staging of axillary lymph nodes, it was included in our study for completeness.
Qualitative and/or quantitative criteria are used to differentiate metastatic from nonmetastatic lymph nodes, as demonstrated in this and other studies (4,5,15–38,40,41,43). By using both criteria in the same lymph node, discrepant results are reported rarely. In our qualitative visual analysis, two (2%) of 122 lymph nodes were rated as false-positive on USPIO-enhanced images. The quantitative analysis, however, showed an SI decrease of more than 55% on T2-weighted fast SE images and on T2*-weighted FFE images, and this decrease indicates nonmetastatic involvement. Although these findings are based on a small number of lymph nodes, we recommend that, in doubtful cases, results of SI measurements before and after USPIO administration should be considered more accurate than the results of the visual analysis. In such a case, a substantial SI decrease in a lymph node should be rated as a sign of nonmetastatic involvement.
There were some limitations to our study. First, because of the small number of metastatic lymph nodes, the full spectrum of the appearance of metastatic nodes is yet to be determined. A larger prospective study should be performed to validate our observation by ascertaining the accuracy of the technique in the detection of nodal metastases. In addition, we did not assess each sequence, plane, and arm position in a blinded reading. Further studies with different imaging analysis protocols are needed to demonstrate that our results of the nonindependent evaluation at nonenhanced and USPIO-enhanced MR imaging were not influenced by a possible selection bias. Second, because of the limits of spatial resolution, metastases of 1 mm or smaller cannot be identified by using this technique. This incapability may not be a significant limitation, as the detection of an occult micrometastasis (defined as smaller than 1 mm) remains controversial and appears to be of limited clinical value (37,44). Third, although the USPIO-enhanced lymph node assessment itself shows very good results, the results are made to appear more promising by means of a comparison with a method that has little clinical value. It is appropriate that nonenhanced MR imaging of the axilla is rarely used in clinical routine. To assess the value of USPIO-enhanced MR imaging, however, a comparative study is necessary to demonstrate a possible benefit of USPIO-enhanced MR imaging of axillary lymph nodes. Finally, because we analyzed MR images from hard-copy films, we were not able to magnify the images for optimal visualization. MR imaging evaluation from a workstation may, therefore, be advantageous.
In conclusion, the results of our study confirm the value of USPIO-enhanced MR imaging as a potential diagnostic tool, on the basis of enhancement patterns, for preoperative nodal staging in patients with breast carcinomas. Imaging findings seen at USPIO-enhanced MR imaging correlate with histopathologic findings, and USPIO-enhanced MR imaging is superior to nonenhanced MR imaging.
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ADVANCES IN KNOWLEDGE |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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FOOTNOTES |
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Abbreviations: FFE = fast field echo • SE = spin echo • SI = signal intensity • SNR = signal-to-noise ratio • 3D = three-dimensional • USPIO = ultrasmall superparamagnetic iron oxide
See Materials and Methods for pertinent disclosures.
Author contributions: Guarantors of integrity of entire study, all authors; 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, M.M., A.K., T.H.H.; clinical studies, M.M., C.C.R., A.G., M.R., T.H.H.; statistical analysis, A.K., W.M.; and manuscript editing, M.M., A.K., A.G., W.M., T.H.H.
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