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Breast Imaging |
1 From the Department of Radiology, University Hospital Policlinico San Donato, 20097 San Donato Milanese, Milan, Italy (F.S., A.I., A.F.); Department of Radiology, "A. Avogadro" University, Novara, Italy (A.C.); and Section of Worldwide Medical Affairs, Bracco Imaging, Milan, Italy (M.A.K.). Received April 22, 2004; revision requested June 30; revision received July 29; accepted August 19. Address correspondence to F.S. (e-mail: f.sardanelli@grupposandonato.it).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: The original study had local ethics committee approval; informed consent was obtained from all enrolled patients. Ninety-five patients known to have or suspected of having breast cancer were randomly assigned to four groups to receive gadobenate dimeglumine at a dose of 0.05, 0.10, or 0.20 mmol per kilogram of body weight or gadopentetate dimeglumine at a dose of 0.10 mmol/kg. T1-weighted gradient-echo MR images were acquired before and 2 minutes after intravenous contrast material injection. Subtracted images were used to obtain maximum intensity projections (MIPs). Two readers blinded to the type and dose of contrast agent administered scored the MIPs obtained in the dose groups for vessel number, length, and conspicuity from 0, which indicated absent or low breast vascularity, to 3, which indicated high breast vascularity. The sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) of one-sided increased vascularity in association with ipsilateral malignancy for 69 histopathologically confirmed lesions (reference standard) were determined after gadobenate dimeglumine–enhanced MR imaging.
RESULTS: The mean MIP scores assigned to the gadobenate dimeglumine groups were significantly higher than those assigned to the gadopentetate dimeglumine group (P 
.044). Histopathologic analysis revealed malignant lesions in 52 of 69 patients examined with gadobenate dimeglumine MR imaging: invasive ductal carcinoma in 45, invasive lobular carcinoma in four, and invasive mixed ductal-lobular carcinoma in three patients. Seventeen patients had benign lesions. Two cases of bilateral invasive cancer with symmetric breast vascular maps were excluded. Thus, the overall sensitivity, specificity, accuracy, PPV, and NPV of one-sided increased vascularity as a finding associated with ipsilateral malignancy were 88% (44 of 50 patients), 82% (14 of 17 patients), 87% (58 of 67 patients), 94% (44 of 47 patients), and 70% (14 of 20 patients), respectively.
CONCLUSION: Gadobenate dimeglumine is effective for MR imaging evaluation of breast vessels at doses as low as 0.05 mmol/kg. One-sided increased vascularity is an MR imaging finding frequently associated with ipsilateral invasive breast cancer.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Since the first use of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) for contrast-enhanced MR imaging of the breast in 1986 (10), clinical breast MR imaging examinations have been performed exclusively with either this agent or similar nonspecific paramagnetic agents. All agents of this type are chelates of the paramagnetic ion gadolinium, and all are characterized by two-compartment pharmacokinetics that reflect their vascular-interstitial biodistribution. All of these agents have similar T1 relaxivities—ranging between 4.3 and 4.8 (mmol/L)–1 · sec–1—so they yield comparable contrast enhancement on T1-weighted breast MR images when injected at equivalent dose (11).
Gadobenate dimeglumine (MultiHance; Bracco Imaging, Milan, Italy) also is a gadolinium-based contrast agent characterized by two-compartment pharmacokinetics (12–14). However, unlike an injected dose of gadopentetate dimeglumine, a small fraction of the injected dose of gadobenate dimeglumine is taken up by functioning hepatocytes, so this agent has a partially hepatobiliary biodistribution (13,14). Furthermore, owing to its capacity for a weak and transient interaction with serum albumin (12), gadobenate dimeglumine has a twofold higher T1 relaxivity in vivo (9.7 [mmol/L]–1 · sec–1) compared with gadopentetate dimeglumine and other conventional gadolinium-based agents. This property has been shown to be advantageous not only for MR imaging of intraaxial lesions of the central nervous system (15) but also for MR angiography (16–19).
The presence of increased blood flow in the breast tumor itself has been demonstrated previously at positron emission tomography (20), at temporally resolved contrast-enhanced MR imaging (with images acquired at intervals of 15 seconds) (21–24), and in a comparison between color Doppler ultrasonography and contrast-enhanced MR imaging (25). Furthermore, increased blood flow in the skin of the breast harboring cancer has been demonstrated by using laser Doppler perfusion (26). More recently, an ipsilateral association between cancer and increased breast vascularity has been demonstrated at MR imaging enhanced with conventional two-compartment gadolinium chelates (27,28).
The aims of this study were to compare three different doses of gadobenate dimeglumine with a standard dose of gadopentetate dimeglumine for the MR imaging evaluation of breast vessels and to evaluate the accuracy of one-sided increased vascularity seen on gadobenate dimeglumine–enhanced MR images as an indicator of ipsilateral breast cancer.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Study Subjects
The present study was a retrospective evaluation of the MR imaging results and pathology records of patients who were enrolled at seven centers in Europe as part of a double-blind, multicenter, randomized phase II dose-finding parallel-group study to compare three different doses of gadobenate dimeglumine with a single dose of gadopentetate dimeglumine for contrast-enhanced MR imaging of the breast (29). Each center in the original study had local ethics committee approval for the study, and written informed consent was obtained from each enrolled patient. Institutional review board approval and written informed consent included approval and consent for the use and publication of any data from the study, with patient confidentiality maintained.
From July 1998 to April 1999, 95 women (mean age, 54.3 years ± 12.0 [standard deviation]; age range, 27–77 years) known to have or suspected of having breast cancer were enrolled, and a total of 95 breast MR imaging examinations were performed (one examination per patient). These patients randomly received either gadobenate dimeglumine at a dose of 0.05 (n = 24), 0.10 (n = 24), or 0.20 (n = 24) mmol per kilogram of body weight or gadopentetate dimeglumine at a dose of 0.10 mmol/kg (n = 23).
MR Imaging
MR imaging was performed by using a 1.5-T unit (Magnetom Vision or Magnetom Symphony; Siemens Medical Solutions, Erlangen, Germany) and a dedicated double-breast coil in all patients while they were in the prone position.
Contrast-enhanced MR images were obtained by using commercially available formulations of 0.5 mol/L gadobenate dimeglumine and 0.5 mol/L gadopentetate dimeglumine. All doses were administered intravenously in a bolus at a rate of 2 mL/sec and were followed by a standardized 20-mL saline flush administered at the same rate. The contrast medium and the saline flush were administered by using a power injector. Contrast-enhanced MR image acquisition started immediately after contrast agent injection, at the end of the saline flush.
MR images were acquired in the coronal plane before (unenhanced) and after (contrast enhanced) contrast agent injection by using a three-dimensional T1-weighted spoiled gradient-echo sequence with fat and water in-phase (echo time between and 4.0 and 4.8 msec in the present study); a repetition time of 13 msec or less; one signal acquired; a rectangular field of view of 36 cm or smaller; a matrix of 128 x 256; a flip angle of 20°–30°; an in-plane resolution of 2 mm2 or less, which covered both whole breasts; with thin (3-mm) partitions but no intersection gap.
A series of five contrast-enhanced MR images were acquired, beginning at 0, 2, 4, 6, and 8 minutes after contrast material injection. Only the first dynamic phase images (acquired at 2 minutes after injection in this study) were considered, so that we had the best "angiographic effect" for both arteries and veins; in fact, in the subsequent acquisitions, a more pronounced distribution of contrast material in the interstitial space reduces the vascular enhancement (11,30). Unenhanced images were subtracted from the contrast-enhanced images on a pixel-by-pixel basis.
Image Analysis
All images were evaluated on the same workstation (MagicView 1000; Siemens Medical Solutions) by using identical software (Numaris; Siemens Medical Solutions). Coronal and transverse maximum intensity projections (MIPs) were prepared from the subtracted MR images for assessment. For the coronal views, the posterior part of the volume was cut from the image to avoid superimposition of the contrast material–filled heart on the left breast. Two off-site readers who had 12 (F.S.) and 4 (A.I.) years of experience in contrast-enhanced breast MR imaging and were blinded to the contrast agent administered, the dose injected, and the results of histopathologic examination performed the image evaluations in consensus and in a randomized manner. They evaluated the coronal and transverse MIPs by using a one-on-one format, free windowing, and electronic magnification and distance measurement.
A score ranging from 0, indicating absent or very low breast vascularity, to 3, indicating high breast vascularity, was assigned to each pair (coronal and transverse) of MIP images on the basis of the number of vessels seen and the length and conspicuity of the vessels. The score was assigned according to the number of vessels per breast that were 3 cm or greater in length and 2 mm or greater in maximal transverse diameter: A score of 0 indicated absent or very low vascularity—that is, the complete absence of vessels or the presence of vessels less than 3 cm in length and less than 2 mm in maximal transverse diameter. A score of 1 indicated low vascularity—that is, only one vessel was 3 cm or greater in length and 2 mm or greater in maximal transverse diameter. A score of 2 indicated moderate vascularity—that is, two to four vessels were 3 cm or greater in length and 2 mm or greater in maximal transverse diameter. A score of 3 indicated high vascularity—that is, five or more vessels were 3 cm or greater in length and 2 mm or greater in maximal transverse diameter. The mean vascularity grade for the two breasts was calculated.
Two months after this evaluation, a second evaluation of the images obtained in the 72 patients who underwent gadobenate dimeglumine–enhanced MR imaging was performed. This evaluation also was performed in consensus and in a randomized manner at the satellite MR imaging workstation by the two readers mentioned earlier (F.S. and A.I.). They were blinded to the contrast agent dose injected and to the histopathologic examination results. Again, the number of vessels that were 3 cm or greater in length and 2 mm or greater in maximal transverse diameter was considered. When the difference in the number of these vessels between the two breasts was two or higher, the vascularity of the breast with the most vessels was considered to be increased compared with the vascularity of the other breast. In such cases, vascular asymmetry and the side of its occurrence were recorded, and the patient was considered to have one-sided increased vascularity. The presence and morphologic features of enhancing nodules were not considered during these evaluations.
Histopathologic Reference-Standard Findings
Of the 72 patients examined at gadobenate dimeglumine–enhanced MR imaging, 69 underwent histopathologic examination of their breast lesion—as the reference standard—after surgical excision (n = 63) or core-needle biopsy (n = 6). Excision or biopsy and subsequent histopathologic examination were performed at each center by local pathologists according to the 1981 World Health Organization breast cancer classification system (31). The remaining three patients opted not to be a part of this protocol and did not undergo surgery or biopsy during the original study. These three patients were therefore excluded from our analyses. Surgery and biopsy were permitted 48 hours to 1 month after MR imaging. When a malignant lesion was found at histopathologic examination of a surgical or core-needle biopsy specimen from the breast with one-sided increased vascularity, according to the findings at blinded evaluation of the MIP maps, vascular asymmetry was considered to be a true-positive associated finding.
The lesion size at histopathologic examination, when reported, was classified in terms of the maximum lesion diameter into one of the following categories: 5 mm or less, greater than 5 mm but less than or equal to 10 mm, greater than 10 mm but less than or equal to 20 mm, greater than 20 mm but less than or equal to 50 mm, and greater than 50 mm. When more than one malignant focus per breast was found, the one that was the largest in diameter in each breast was considered for the current analysis.
Statistical Analyses
Results were evaluated statistically by using nonparametric Kruskal-Wallis and two-tailed Mann-Whitney U tests. Kruskal-Wallis testing was used for global variability analysis of the angiographic scores assigned to the MIPs obtained in patients in the four dose groups (0.05, 0.10, and 0.20 mmol/kg gadobenate dimeglumine and 0.10 mmol/kg gadopentetate dimeglumine), and two-tailed Mann-Whitney U testing was used for post hoc intergroup comparisons of angiographic scores (SPSS for Windows, release 6.0; SPSS, Chicago, Ill). Kruskal-Wallis testing was also used for global variability analysis of the age and size of the malignant lesions in the four dose groups. The middle value in the lesion size classification system was considered to represent the size of all lesions with a diameter of greater than 5 mm but less than or equal to 50 mm, whereas 2.5 mm was considered to represent the size of lesions with diameters of less than or equal to 5 mm and 75 mm was considered to represent the size of lesions with diameters greater than 50 mm. Thus, the lesion sizes considered were 2.5, 7.5, 15.0, 35.0, and 75.0 mm. P < .05 was considered to indicate a significant difference.
The sensitivity, specificity, positive predictive value, and negative predictive value of one-sided increased breast vascularity as an indicator of ipsilateral invasive breast cancer were calculated. Corresponding 95% confidence intervals were calculated by using the Fisher exact method (32).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Of all patients in the four dose groups combined, 68 (70 breasts because of two bilateral tumors) had cancer. The mean maximum diameter of the main malignant lesion, as reported at histopathologic examination for 59 of these 68 patients (61 of 70 breasts), was 24.0 mm ± 18.7 (standard deviation). There was no significant difference (P > .05, Kruskal-Wallis test) in the mean size of the main malignant lesion between the different dose groups in which the lesion diameter was reported after histopathologic examination: 23.8 mm ± 19.7 for the 0.05 mmol/kg gadobenate dimeglumine group (n = 15), 25.7 mm ± 20.5 for the 0.10 mmol/kg gadobenate dimeglumine group (n = 14), 20.6 mm ± 14.0 for the 0.20 mmol/kg gadobenate dimeglumine group (n = 13), and 25.0 mm ± 20.3 for the 0.10 mmol/kg gadopentetate dimeglumine group (n = 17).
Vascular Maps and Contrast Agents
The mean scores assigned to the vascular maps obtained with gadobenate dimeglumine–enhanced MR imaging at 0.05, 0.10, and 0.20 mmol/kg doses were 1.90 ± 1.07, 1.94 ± 0.95, and 2.00 ± 0.75, respectively. The corresponding mean score assigned to maps obtained with 0.10 mmol/kg gadopentetate dimeglumine–enhanced MR imaging was 1.24 ± 0.84 (Fig 1). Global variability analysis performed with the Kruskal-Wallis test revealed significant differences (P = .018) in vascular map scores. Post hoc analysis performed by using the Mann-Whitney U test revealed significantly higher scores for each of the gadobenate dimeglumine dose groups compared with the score for the gadopentetate dimeglumine dose group (P = .044, P = .009, and P = .002, respectively, for 0.05, 0.10, and 0.20 mmol/kg gadobenate dimeglumine groups vs 0.10 mmol/kg gadopentetate dimeglumine group).
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Asymmetric breast vascularity due to the presence of one-sided increased vascularity was observed in 47 of the 67 patients examined with gadobenate dimeglumine–enhanced MR imaging. In 44 (94%) of these 47 patients, the increased vascularity was associated with histopathologically proved ipsilateral breast cancer. These were considered to be true-positive cases. The sizes of only 36 lesions in these 44 true-positive cases were reported at histopathologic analysis: One lesion was 5 mm or smaller, seven were larger than 5 mm but smaller than or equal to 10 mm, 12 were larger than 10 mm but smaller than or equal to 20 mm, 14 were larger than 20 mm but smaller than or equal to 50 mm, and two were larger than 50 mm. The sizes of the lesions in the remaining eight patients with true-positive lesions were not reported by the investigating pathologists.
The three patients with one-sided increased vascularity who were shown not to have cancer at histopathologic examination of the suspicious lesion in the ipsilateral breast were considered to be false-positive cases. Their lesions comprised a 7-mm area of papillomatosis in the 0.10 mmol/kg gadobenate dimeglumine group and an 8-mm papilloma and a 15-mm area of hyperplasia in the 0.20 mmol/kg gadobenate dimeglumine group.
Considering one-sided increased vascularity as a finding associated with ipsilateral breast cancer led to the recording of six false-negative cases among the 67 patients examined with gadobenate dimeglumine–enhanced MR imaging, with the two patients with bilateral cancers excluded. All six of these false-negative lesions were invasive ductal carcinomas and were identified in each of the three dose groups: One, three, and two lesions were identified in the 0.05, 0.10, and 0.20 mmol/kg gadobenate dimeglumine groups, respectively, and one of these lesions had a large intraductal component. Only two of these six false-negative lesions were 10 mm or smaller. The remaining false-negative lesions comprised two foci larger than 10 mm but smaller than or equal to 20 mm and two foci larger than 20 mm but smaller than or equal to 50 mm. Of 36 invasive cancers for which the size was reported at histopathologic examination, eight were minimal (10 mm in diameter) and 28 were not minimal (>10 mm in diameter). Ipsilateral increased vascularity was detected for six (75%) of eight minimal cancers and 24 (86%) of 28 nonminimal cancers. Consequently, two (25%) of the eight minimal cancers and four (14%) of the 28 nonminimal cancers were false-negative cases.
A cross tabulation of the results of the analysis of one-sided increased breast vascularity as a predictor of ipsilateral invasive breast cancer versus the histopathologic results is presented in Table 1. The sensitivity, specificity, positive predictive value, and negative predictive value of one-sided increased vascularity as an indicator of ipsilateral invasive breast cancer, with corresponding 95% confidence intervals, are reported in Table 2.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Our experience revealed that MR imaging with gadobenate dimeglumine administered at doses as low as 0.05 mmol/kg enables high-quality vascular maps of the breast to be obtained and that the angiographic effect at this and higher doses is significantly greater than the effect following the administration of a standard 0.10 mmol/kg dose of gadopentetate dimeglumine. These findings are in agreement with those in previous MR angiography studies of other vascular territories examined with gadobenate dimeglumine enhancement (16–19). Our findings also suggest that vascular map asymmetry may be a finding that is frequently associated with ipsilateral invasive breast cancer: Sensitivity and specificity values of 88% and 82%, respectively, suggest that vascular asymmetry could be considered a corollary MR imaging sign of invasive breast cancer.
The small number of false-negative cases (n = 6) in this study precluded an accurate comparison between the dimensions of cancers associated with ipsilateral vascular prevalence and the dimensions of cancers not associated with this feature. However, it is noteworthy that at histopathologic examination, at least eight of the 44 true-positive lesions had a diameter of 10 mm or smaller, while four of the six false-negative lesions were larger than 10 mm and only two were smaller than or equal to 10 mm. These findings suggest that the dimension of the cancer probably is not the key factor in the ipsilateral prevalence of increased breast vascularity. Despite the small number of false-negative lesions, the roughly even distribution of these foci among the three dose groups is not indicative of a dose-related trend.
The presence of ipsilateral breast vascular prevalence in association with cancer may be due to reduced flow resistance in the tumor vessels, the tumor’s higher metabolism, angiogenic stimulation of the whole breast, or a combination of these factors. In our opinion, the first two possibilities may have a role in determining whole-breast increased vascularity when the cancer is relatively large in comparison with the dimension of the breast. Conversely, angiogenic stimulation of the whole breast by the tumor is more likely when the cancer is small. The role of neoangiogenic peptides in the prognosis of breast cancer remains an area of active research (33,34).
Previously, ipsilateral vascular prevalence in association with cancer was studied exclusively with gadopentetate dimeglumine. Mahfouz et al (27) administered 0.10 mmol/kg gadopentetate dimeglumine in 106 randomly selected patients—85 had unilateral malignant lesions, and 21 had unilateral benign lesions—and obtained sensitivity, specificity, accuracy, positive predictive, and negative predictive values of 77% (65 of 85 patients), 57% (12 of 21 patients), 73% (77 of 106 patients), 88% (65 of 74 patients), and 38% (12 of 32 patients), respectively, based on asymmetric vascular maps. More recently, Carriero et al (28) administered 0.20 mmol/kg gadopentetate dimeglumine in 101 patients— 78 with unilateral malignant lesions and 23 with unilateral benign lesions—and obtained sensitivity, specificity, accuracy, positive predictive, and negative predictive values of 72% (56 of 78 patients), 100% (23 of 23 patients), 78% (79 of 101 patients), 100% (56 of 56 patients), and 51% (23 of 45 patients), respectively.
Although the prevalences of breast cancer in our study and in the Mahfouz et al (27) and Carriero et al (28) studies were similar (approximately 75% vs 80% and 77%, respectively), greater overall accuracy was achieved in our study (87% vs 73% and 78%, respectively) mainly owing to our higher sensitivity and negative predictive values: 88% and 70%, respectively, in our study versus 77% and 38%, respectively, in the Mahfouz et al study and 72% and 51%, respectively, in the Carriero et al study. It seems reasonable to assume that this improved accuracy is related to the greater angiographic effect of gadobenate dimeglumine (compared with the angiographic effect of gadopentetate dimeglumine), which in turn is related to the greater T1 relaxivity of gadobenate dimeglumine. The improved performance of gadobenate dimeglumine–enhanced MR imaging compared with the performance of gadopentetate dimeglumine–enhanced MR imaging in the detection and characterization of breast lesions was observed previously in the original phase II clinical trial (29).
Several limitations of our study should be taken into account. First, the evaluation of breast vascular maps was performed without masking the enhancing lesions. Although this may have introduced bias in terms of the assessment of side-based prevalence of vascularity when the vascular asymmetry was around the cutoff point, it should be noted that the evaluation procedure was similar to that performed daily in routine clinical practice. Second, our series did not include any patients with pure in situ carcinomas, which are known to have reduced angiogenesis compared with invasive carcinomas (35). However, five invasive carcinomas with large intraductal components were included, and four (80%) of them were considered to be true-positive for asymmetric breast vascularity. Nevertheless, the predictive value of asymmetric breast vascularity for in situ carcinomas remains to be investigated.
A further limitation, which was due to the retrospective nature of this study, was the absence of follow-up information on one-sided decreased vascularity to confirm the true-negative cases of breast vascular asymmetry. Similarly, no information on the remaining portion of the breast after surgery or core-needle biopsy was available to exclude the possible true-positive cases of one-sided increased vascularity in those patients who were deemed to have false-positive lesions on the basis of the benignancy of the suspicious lesion after either surgery or biopsy. For these reasons, our observation of a frequent association between one-sided increased breast vascularity and ipsilateral breast cancer cannot be immediately applied to the general female population.
It should also be noted that the percentages of false-negative breast vascular maps in the presence of invasive cancers of minimal (10 mm in diameter) or nonminimal (>10 mm in diameter) size suggest a 25% probability of false-negative (symmetric) breast vascular maps when the invasive cancer is minimal and a 14% probability of false-negative (symmetric) breast vascular maps when the invasive cancer is not minimal; these probabilities should be taken into account in clinical practice. At present, we do not know if the associated finding of one-sided increased vascularity increases the sensitivity and/or the specificity of contrast-enhanced breast MR imaging, in which accuracy is based on standard morphologic and dynamic criteria, in a large population of women. This would be an extremely interesting finding, particularly if the rate of positive cases observed by using conventional criteria was lower than that observed in the current study.
Finally, it would be interesting to determine whether the association between one-sided increased vascularity and ipsilateral breast cancer is also apparent with the use of gadopentetate dimeglumine and other conventional MR imaging contrast agents or whether it is more apparent with the use of gadobenate dimeglumine owing to this agent’s higher in vivo relaxivity and preferential properties for MR angiography (16–19). The small number of cases studied with single-dose gadopentetate dimeglumine (n = 23) in the current study precluded a meaningful comparative evaluation with this agent. On the other hand, results of previous studies (27,28) have suggested that gadopentetate dimeglumine also may be appropriate for depicting ipsilateral higher vascularity.
In conclusion, our results suggest that gadobenate dimeglumine, as compared with gadopentetate dimeglumine, may have preferential properties for MR imaging evaluation of breast vascularity and that one-sided increased breast vascularity is frequently associated with ipsilateral invasive breast cancer. However, further work is clearly warranted to assess the additional value of vascular asymmetry as a sign of breast malignancy, as compared with the value of established dynamic and morphologic criteria. Additional work should be focused not only on patients with invasive cancer but also on patients with in situ cancers and in a larger population of women with benign lesions or no lesions.
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FOOTNOTES |
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See Materials and Methods for pertinent disclosures.
See also Science to Practice in this issue.
Author contributions: Guarantor of integrity of entire study, F.S.; study concepts, F.S., A.I., A.C.; study design, all authors; literature research, A.F.; clinical studies, A.C.; data acquisition, F.S., A.I., M.A.K.; data analysis/interpretation, F.S., A.I., A.F.; statistical analysis, F.S., A.F.; manuscript preparation, F.S., A.F.; manuscript definition of intellectual content, revision/review, and final version approval, all authors; manuscript editing, F.S., A.F., M.A.K.
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