Whole-Body Positron Emission TomographyMagnetic Resonance in Breast Cancer Andrew Sher, MD, Laia Valls, MD, Raymond F. Muzic Jr, PhD, Donna Plecha, MD, and Norbert Avril, MD

Whole-Body Magnetic Resonance Technology

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ybrid positron emission tomography (PET)-magnetic resonance (MR) technology has recently been introduced into the market, appearing in the clinical setting in 2007.1,2 Whether designed as a sequential or simultaneous system, the hybrid PET-MR produces high-resolution anatomical, biological, and functional imaging. Given the limited approved indications of PET/computed tomography (CT) in patients with breast cancer, it is understandable that the potential role of PET-MR in such patients remains to be determined. The impetus to develop whole-body MR imaging (WB-MRI) scanning techniques lies in its advantages over CT. Namely, MRI makes no use of ionizing radiation, provides exceptional soft tissue contrast, and offers the ability to perform multisequence and multiplanar imaging, which allows for improved lesion characterization. The feasibility of a hybrid PET-MR scanner to evaluate the WB was dependent on the development of WB-MR sequences that could be conducted within a reasonable period while providing diagnostic images. The development of such sequences has been made possible by hardware innovations including multireceiver channel WB scanners as well as acquisition acceleration techniques.3 Such advances allow the assessment of multiple organ systems during 1 scan to be conducted in an efficient and clinically applicable manner.3,4 In terms of clinical applications, WBMRI holds promise in evaluating tumors with frequent metastatic spread to the bone, liver, and central nervous system, such as lung cancer, colorectal cancer, prostate cancer, melanoma, and definitively breast cancer.3 The recent advent

Department of Radiology, University Hospitals Case Medical Center, Case Center for Imaging Research, Case Western Reserve University, Cleveland, OH. Address reprint requests to Norbert Avril, MD, Department of Radiology, University Hospitals Case Medical Center, Case Center for Imaging Research, Case Western Reserve University, 11100 Euclid Ave, Cleveland, OH 44106. E-mail: [email protected]

http://dx.doi.org/10.1053/j.ro.2014.08.001 0037-198X/& 2014 Elsevier Inc. All rights reserved.

of WB-MRI Dixon-based sequences has further reduced the time necessary for WB scans.5 Moreover, with the introduction of diffusion-weighted imaging (DWI), which identifies tumors based on the restricted diffusion of water molecules owing to their increased nuclear-cytoplasmic ratio and hypercellularity,6 it also improved the sensitivity for lesion detection. This is particularly helpful in using the WB-DWI with background body signal suppression (DWIBS) under free breathing, which overcomes the challenges offered by breath holding and respiratory triggered scanning, and allowing for thin slices with multiple signal averaging within an efficient acquisition time.7 Although early work with DWI in patients with breast cancer has shown potential in evaluating axillary lymph nodes,8 WB-DWI alone cannot be recommended as a WB staging alternative given its high false-positive rate.9 Thus, the combination of DWI with conventional sequences has been shown to increase the sensitivity and specificity of WB-MRI,10 and a promising area of research is how the metabolic information of fluorodeoxyglucose (FDG)-PET can be used with DWI (Fig. 1). Taken together, the advances in WB-MRI has been an invaluable step in the maturation of hybrid PET-MR systems. Regardless of whether the hybrid PET-MRI system acquires images in a sequential or simultaneous fashion, dedicated MRI sequences are used for attenuation correction of PET data, a necessary step to account for differences in the attenuation of photons by different tissues of the body. Precise and reproducible attenuation correction is necessary to determine accurate quantification of FDG activity and allow for standardized uptake value (SUV) reporting. In PET/CT, attenuation coefficients of tissues at x-ray energies are obtained from the CT data itself, which directly provides data to allow for maps to 511-keV photon attenuation coefficients.11 As MR images are determined by tissue hydrogen density and relaxation properties, the data cannot be directly converted into attenuation maps. Instead, MR attenuation maps rely on automated tissue segmentation methods.12,13 Despite the differences in attenuation methods between PET/CT and PET-MR, initial studies to date have shown both 313

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overall good correlation between SUV values and similar detection rates between the 2 modalities.14-16 The most significant differences in SUV values tend to be seen in osseous lesions17,18 likely explained by current segmentation models not accounting for bone attenuation.12,13 PET/CT is now established as the imaging modality of choice in many clinical conditions, particularly in oncology.19 It has to be noticed that a hybrid PET-MRI examination can generate more than 10,000 slices not all of which would necessarily cover the whole field of view or be isotropic, as opposed to modern multislice PET/CT data. As of today, although PET-MRI provides unparalleled structural, metabolic, and functional information, an improvement in diagnostic accuracy, a change in management, or a change in patient outcome has not been demonstrated compared with PET/CT. In the clinical routine, more integrated PET-MRI considerations and protocols will need to be improved to optimize their workflow and imaging protocols.20

FDG-PET WB Staging

Figure 1 Metastatic breast cancer in a 63-year-old woman. (A) Diffusion-weighted MR image, obtained with a b value of 1000, demonstrates multiple foci of diffusion restriction (arrowheads). (B) Axial FDG-PET images obtained at the same level demonstrate 2 intense hypermetabolic foci; the remainder of the lesions seen in (A) are not well appreciated above background hepatic uptake. (C) Fused FDG-PET-MR images clearly illustrate the extent of disease. (Color version of figure is available online.)

The introduction of integrated PET/CT systems led to an increase in diagnostic confidence and accuracy of restaging patients with suspected metastasis.21 Furthermore, in patients previously treated for breast cancer and presenting with suspected recurrence, FDG-PET/CT has proven to be highly sensitive, specific, and accurate.22-24 Multiple studies have sought to evaluate the effectiveness of FDG-PET and FDGPET/CT on staging and management of patients with breast cancer.22,25-28 Yap et al found that FDG-PET resulted in changes in clinical stage in 36% of the patients. Furthermore, in 53% of those patients whose stage was not altered by FDGPET, management was changed because of the additional information provided.26 These results are concordant with those from Mahner et al28 who found that FDG-PET is superior to conventional imaging for the detection of distant metastases. Although FDG-PET has shown a higher sensitivity than conventional imaging in the detection of metastatic disease, the effect of increased sensitivity on patient care and outcome has not been demonstrated.29 Furthermore, prior studies of patients with stage I or early stage II disease have demonstrated that extensive imaging examinations are unnecessary in most patients with newly diagnosed breast cancer and result in a high degree of false positives and associated economical and emotional distress of patients.30 Per the current National Comprehensive Cancer Network guidelines, when imaging is recommended for staging, CT or bone scintigraphy or both are the initial studies of choice. However, at the early stage of disease, lesions may remain invisible in the absence of an osteoblastic response. Furthermore, misinterpretation of tracer uptake in healing fractures or degenerative disease may lead to false-positive findings.14 FDG-PET/CT is currently helpful in situations where standard staging studies are equivocal or suspicious, especially in the setting of locally advanced or metastatic disease.31

Whole-body PET-MR in breast cancer Veit-Haibach et al examined 44 patients with suspicion of recurrent breast cancer comparing PET/CT, PET alone, and CT alone for diagnostic accuracy and influence on therapy. The authors found that combined PET/CT was more accurate in assessing TNM staging and had a moderate effect on therapy compared with PET and CT. Tumor stage was correctly determined in 91% of cases with PET/CT, compared with 81% of cases with PET alone or contrast-enhanced CT alone, leading to a consequent change of therapy.22 Murakami et al24 examined 47 patients with suspected recurrent breast cancer and found FDG-PET/CT had a sensitivity, specificity, and accuracy of 96%, 91%, and 94%, respectively. Despite these findings, FDG-PET/CT is currently recommended by the National Comprehensive Cancer Network guidelines as an adjunct to conventional imaging when standard studies are equivocal or suspicious for recurrent disease.31 As described previously, dedicated breast MRI has been shown to be highly sensitive, detecting lesions that are occult to mammography, ultrasound, and clinical breast examination, though lacking in specificity.32 Alternatively, FDG-PET/CT has been shown to have a higher specificity than MRI in detecting breast cancer recurrence.33 Iagaru et al33 studied 21 patients with known breast cancer and concluded that PET/CT and breast MRI should be considered as complimentary imaging tools. Goerres et al34 examined 32 patients with suspected locoregional breast cancer recurrence or suspected contralateral breast cancer and found that the combination of FDGPET and breast MRI would result in a sensitivity and specificity of 93% and 94%, respectively. Nevertheless, it has yet to be shown that FDG-PET can add specificity to MR in lesions that have previously been shown to have low detectability on FDGPET, including those that lie below the spatial resolution of the system or have low metabolic activity.35 Combining the lack of radiation, extraordinary soft tissue contrast, and high spatial resolution of MRI multiparametric techniques (DWI, dynamic contrast-enhanced imaging, and MR spectroscopy) with the metabolic information provided by FDG-PET yields accurate WB staging or restaging examinations. Consequently, FDG-PET-MRI will be best suited for clinical situations that are disease specific or organ specific, especially in children or patients requiring repeated imaging to achieve a low cumulative radiation dose. It may also enhance patient convenience by providing a “one-stop shop” diagnostic imaging workup, reducing patient anxiety, total scan time, and potential recalls for repeat scanning.19 Furthermore, in patient populations in which differentiation of highly cellular hematopoietic marrow and neoplasm is difficult, FDG-PET-MR could potentially aid in diagnosis and provide information on the aggressiveness of such lesions.3 Prior studies have shown WB-MRI to be a feasible modality in detecting metastatic disease to the bone, brain, and liver,36,37 sites which breast cancer frequently metastasizes to (Fig. 2). A study of 51 patients with known malignancy compared WBMRI with the reference techniques of CT and bone scintigraphy to evaluate soft tissue and bony metastases. The authors found that WB-MRI was comparable to CT and bone scintigraphy in detecting metastases and was more sensitive

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Figure 2 Metastatic breast cancer in a 71-year-old woman. (A) Contrast-enhanced Dixon fat-suppressed axial MR image demonstrating a cystic cavity lesion (arrow) corresponding to a recurrent metastasis following ablation. There is a subtle lesion appreciated behind the main portal vein (arrowhead). (B) Axial FDG-PET images obtained at the same level clearly exhibit 2 intense hypermetabolic foci. (C) Fused FDG-PET-MR images demonstrate the 2 lesions, illustrating the utility of the combination of both techniques. (Color version of figure is available online.)

in detecting hepatic and osseous metastases than the reference techniques.37 The potential benefit of a hybrid PET-MR modality can be seen in a study by Schmidt et al. The authors

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compared WB-MRI with FDG-PET/CT in 33 patients with breast cancer presenting with suspicion of recurrence by evaluating the diagnostic accuracy of local recurrence, lymph node involvement, and distant metastatic disease. The 2 modalities each demonstrated high overall diagnostic accuracy (91%), with sensitivity of 91% (PET/CT) and 93% (WB-MRI), specificity of 90% (PET/CT) and 86% (WB-MRI). PET/CT detected more lymph node metastasis than WB-MRI (96% accuracy vs 75%), whereas WB-MRI demonstrated more metastases to the liver and bone, and similar detection accuracy of pulmonary metastasis (Fig. 3).38 The results of the study are in line with a previous prospective study looking at 98 oncologic patients undergoing both WB-MRI and FDG-PET/ CT, with the exception that MRI was less sensitive to PET/CT in detecting lung metastases.39

Osseous Metastases Metastatic disease to the bone is the most frequent site for distant metastatic disease in patients with breast cancer and accounts for approximately 65% of patients with distant metastases.40 Although bone scintigraphy remains the standard of care for evaluating patients with breast cancer with bone pain, FDG-PET and FDG-PET/CT have been extensively studied in the evaluation of osseous structures for metastatic disease. Initial reports found FDG-PET to have equal sensitivity (78%) to bone scans with a statistically significant improvement in specificity (98% vs 81%).41 Further evaluation demonstrated FDG-PET to be superior to bone scintigraphy in osteolytic lesions but inferior in the detection of osteoblastic lesions.42-44 A study of 163 patients with breast cancer compared the efficacy of FDG-PET/CT with bone scintigraphy in patients with suspected osseous metastases and found a high concordance between the 2 modalities, concluding that FDGPET/CT may be used for the detection of osseous metastatic disease.45 A recent meta-analysis of 668 patients encompassing 7 studies sought to evaluate the accuracy of FDG-PET/CT in comparison with bone scintigraphy for the detection of bone metastases. The pooled sensitivities of FDG-PET/CT and bone scintigraphy were 93% and 81%, respectively, whereas the pooled specificities were 99% and 96%, respectively. The authors concluded that FDG-PET/CT tends to have higher sensitivity and accuracy than bone scintigraphy.40 Despite the favorable results of FDG-PET/CT compared with bone scintigraphy, prospective trials are needed to fully delineate its role; bone scintigraphy remains the mainstay in the diagnostic workup of osseous disease in patients with breast cancer. Bone is the most common site of osseous metastases from breast cancer, seen in 8% of such patients and 69% of patients with advanced disease.46 Given this high rate of osseous metastases, the ability to accurately and reliably detect such lesions is essential for clinical acceptance of hybrid PET-MR and deserves special attention. As an individual modality, WBMRI has been shown to reliably detect osseous metastases by allowing for the visualization of metastatic disease without relying on marked bony reaction or metabolic changes. Early studies demonstrated WB-MRI to have a higher sensitivity,

Figure 3 Metastatic breast cancer in a 57-year-old woman: (A) contrastenhanced Dixon fat-suppressed axial MR image demonstrates a subtle, nonspecific lung nodule within the medial left lower lobe (arrow); (B) axial FDG-PET images obtained at the same level show mild to moderate hypermetabolic uptake within the nodule; and (C) fused FDG-PET-MR images show the uptake corresponds to the subtle nodule, suspicious for metastatic disease and confirmed with follow-up. (Color version of figure is available online.)

specificity, and accuracy than bone scintigraphy in detecting osseous metastases, as well as identifying sites of additional metastatic disease in other organ systems.36,47 A more recent meta-analysis of 7 studies involving 332 patients found that WB-MRI and bone scintigraphy have similar overall sensitivity (84% vs 83%, respectively) and specificity (96% vs 94%, respectively), with neither modality being clearly superior.48

Whole-body PET-MR in breast cancer Another recent meta-analysis conducted by Wu et al49 demonstrated a high sensitivity of WB-DWI to detect bone metastases in expenses of specificity. Causes for false-positive findings on WB-DWI include bone marrow edema caused by fractures, osteoarthritis, infection, bone infarcts, vertebral hemangiomas, isolated bone marrow islands, and bone marrow hyperplasia due to granulocyte colony-stimulating factor. Many of them can be overcome by correlating high bvalue DW images with corresponding apparent diffusion coefficient (ADC) maps and conventional MR sequences based on T1-weighted (T1W) or T2W images. In contrast, causes for false-negative findings include low levels of bone marrow infiltration such as in smoldering multiple myeloma or when background bone marrow hyperplasia obscures the presence of metastases, as well as successfully treated malignant disease and sclerotic metastases.50 In general, lytic or infiltrative lesions are better detected than sclerotic or treated lesions on WBDWI. Moreover, the detection of skeletal metastases on coronal WB-DWI images may be impaired in areas such as the ribs and sternum owing to motion artefacts of respiration. To overcome this challenge, the use of fast turbo spin-echo sequences in combination with axial slicing is recommended.14 Besides, WB-DWI is better at detecting skeletal lesions from smaller cancer cell infiltrations, including breast cancer. There is limited data comparing WB-MRI with FDG-PET/ CT in the workup of osseous metastases. Schmidt et al51 investigated 28 patients with suspected skeletal metastases in which the gold standard was radiological follow-up within 6 months. The authors found that WB-MRI had a higher diagnostic accuracy than PET/CT (91% vs 78%) and was able to detect smaller malignant bone lesions than PET/CT. A more recent prospective study of 13 patients with breast cancer with known or suspected bone metastases compared WB-MRI and FDG-PET/CT. The study used a 3-T magnet, as seen on today's PET-MR hybrid scanners, and included both standard T1W short TI inversion-recovery and DWI techniques. The authors concluded that the combination of T1 and short TI inversion-recovery sequences yielded a combined sensitivity and specificity of 93% and 85%, respectively. However, PET/ CT was used as the gold standard as opposed to follow-up or pathology, which somewhat limits the interpretation of the results.10 Early studies aimed at detecting osseous lesions with hybrid PET-MR systems have been conducted with promising results. Eiber et al examined 119 patients with FDG-avid primary malignancies and compared lesion detectability between PET-MR and PET/CT. The authors found that no significant difference in the classification of malignant bone lesions occurred between PET/CT and PET-MR and that PET-MR was superior to PET/CT for anatomical delineation and allocation of bone lesions.52 Furthermore, the SUVs of PET-MR and PET/CT have been shown to be highly correlated in both bone lesions and normal bone.53,54 Nevertheless, as current attenuation algorithms for PET-MR disregard cortical bone in the attenuation map and thus significantly affect quantitation of FDG uptake,55,56 the SUV values between PET-MR and PET/CT for bony lesions are not interchangeable.53-55

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Treatment Response Given that multiple cycles of treatment are often needed before conventional imaging can detect a change in tumor size,57 the prospect of using early metabolic changes to predict treatment response has been explored. Studies have shown that clinical management regimens based on FDG-PET can avoid multiple treatment cycles of ineffective chemotherapy, as nonresponders can be differentiated quicker and changed earlier to a second line of chemotherapy.58 This in turn saves morbidity and costs for the patient. A recent study in 55 patients with triple-negative breast cancer was conducted to explore the value of PET/CT and dynamic contrast-enhanced MRI in predicting pathological response (pCR) after 2 cycles of neoadjuvant chemotherapy of breast cancer and the dependency on breast cancer subtype. They found that a cutoff of 42% of SUVmax decrease in the primary tumor offered an accuracy of 74% in predicting pCR and relapse. Those results permitted the identification of poor metabolic responders, allowing an early change in treatment plan. They also ascertained significant correlation between high 18FDG uptake (SUVmax) at baseline and pCR in patients with triple-negative breast cancer. On the contrary, residual uptake at interim PET was the most accurate predictive factor in HER2þ patients. Their findings on the ability of interim PET to predict pathology outcomes have been recently confirmed by Koolen et al59 but not by Humbert et al,60 although both of them assessed response after only 1 cycle of neoadjuvant chemotherapy. However, the optimal timing for FDG-PET and the thresholds for relative changes in FDG uptake (SUV) to distinguish between responders and nonresponders has not been established. Such a standard would be essential in incorporating FDG-PET/CT for treatment monitoring into standard clinical practice. Bone scintigraphy is part of the current methods of assessing metastases response to treatment in patients with breast cancer. However, its use is not recommended in assessing early treatment responses because of the scintigraphic or healing flare within 3 months in responders. To overcome falsepositive bone scan lesions, a semiquantitative estimate of skeletal 99mTc-methylene diphosphonate uptake could be useful.50 Up to date, functional imaging techniques such as WB-DWI (using high b-value images together with corresponding ADC values) combined with anatomical imaging (conventional sequences) and other emerging “wet” biomarkers can improve the assessment of nonresponders by monitoring changes in signal intensity abnormalities. Based on experience of the Padhani et al group, ADC increases 41400-1500 mm2/s are rarely seen with disease progression unless there is de novo tumor necrosis. However, the cutoff threshold should be determined depending on the imaging acquisition protocol acquired, as comparison of DW-MRI data acquired between different equipment manufacturers may not always be straightforward. Different response patterns of ADC have been described in their article, as soon as within 1-3 months after instituting therapy.50

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318 To do more accurate volumetric segmentations of deriving “viable tumor volume,” and to minimize “T2 shine-through” effects in heterogeneous lesions, it is recommended to adjust image contrast using ultrahigh b-value images when drawing volume of interest definitions. Besides, threshold ADC histograms can be used to evaluate within more complex changes in ADC data, establishing cutoff values to distinguish between normal and abnormal bone marrow and abnormal bone marrow and nonviable necrotic tumor. These changes may be also depicted calculating the spread of the ADC data as well as with relative frequency histograms, which allows for acknowledgment of the skewness (a measure of the degree of asymmetry of a distribution) and kurtosis (the degree of peakness of a distribution) which are difficult to assess on visual inspections of ADC pixel maps. Finally, the ADC parametric response map is an alternative method that enables to appreciate changes in ADC values at voxel level.50 However, it should be noticed that correct patient positioning and WB image registration between different temporal studies are mandatory to assess ADC changes when the aforementioned methods are applied. This explains their usefulness in diffuse bone metastatic disease, because of spine stillness. A standardized or reliable method of quantifying total burden or of evaluating the response of bony metastases to treatment has not yet been established.61 Nor has the use of WB-DWI been proven yet to clinically affect outcomes in patients with bony metastases.50 Despite encouraging reports about WB-DWI, further prospective studies have to be developed and tested to validate MRI therapy response criteria.

Future Advances of PET-MR in Breast Cancer It is expected that advances in hybrid PET-MR technology will continue and the utility of such imaging in breast cancer patients will evolve. Future directions include combining MRI sequences (including DWIBS) with more conventional sequences to increase the sensitivity and specificity of WBMRI, and a promising area of research is how the metabolic information of FDG-PET can be used with DWIBS. Another area of potential advancement in PET-MR is the development of new methods for accurate MR attenuation. Significant issues still need to be addressed, ranging from metal artifacts (misleading the image segmentation procedure and resulting in severely underestimated uptake), PET-MRI misregistration, lowered uptake in bone, nonrecognition of lung compartment, truncation artifacts and nonuniformities at the edge of the field of view, motion artifact from patient respiration62 as well as the lack of bone in clinically used attenuation-map algorithms.12,13 Interesting work is already being done in these areas, ranging from the implementation of continuous table motion during a PET-MR scan,63 techniques to recover the truncated part of the field of view64,65 because of differences in the respiratory state, acquisition of the attenuation sequence in end expiration to achieve better alignment, referring to the attenuation map and the non-attenuation corrected images, and

development of new attenuation algorithms which account for cortical bone via use of ultrashort echo-time and Dixon sequences.66 Readers should also be advised of the gaining widespread acceptance of the PERCIST criteria.67 It is worth mentioning briefly the potential that new PET biomarkers hold for PET-MRI. Such agents, including those that quantify receptor expression, cell proliferation, and angiogenesis, are an active area of research. These markers, in combination with the high soft tissue and spatial resolution of MRI, seek to improve staging information of patients and the evaluation of therapeutic effectiveness.68

Conclusion The strength of FDG-PET/CT lies in its high sensitivity and specificity in detecting the extent of metastatic disease, often being used when standard staging studies are equivocal or if a previously treated patient with breast cancer becomes symptomatic for recurrence. The recent advent of hybrid PET-MRI systems has created a promising development in the diagnostic options of clinicians caring for patients with breast cancer. Combining the high resolution and soft tissue contrast provided by MRI with the high specificity of metabolic FDGPET information, the potential exists for progress in the management of patients with breast cancer. Early results comparing FDG-PET-MR with FDG-PET/CT in oncologic patients have shown that hybrid PET-MR potentially contributes to clinical management more often than PET/CT.69 Furthermore, image quality, alignment, and confidence in lesion localization appear to be comparable between the 2 modalities.70,71 Although quantification of FDG uptake between the 2 hybrid modalities has been shown repeatedly to be well correlated, semiquantitative analysis using SUVs does show statistically significant differences between PET/CT and PET-MR that need to be considered.53-55 The precise role of PET-MR in breast cancer management, like many oncologic processes, is yet to be determined. Perhaps the use of such a modality remains in the realm of research. Alternatively, PET-MR mammography combined with WB PET-MR staging perhaps could become a so-called one-stop shop for the clinical diagnosis and staging of breast cancer. Advances in technology, including the development of new MR attenuation methodologies, scanner equipment, and new PET radiotracers, are constantly occurring and further delineating the role of PET-MR. Potentially, WB-DWI could make a significant effect in the therapy assessments of patients with metastatic breast cancer.50 Future prospective research trials targeted toward the comparison of PET-MR with today's standard of care imaging for patients with breast cancer will prove extremely worthwhile.

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Whole-body positron emission tomography-magnetic resonance in breast cancer.

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