Original Articles. Depletion of Core Needle Biopsy Cellularity and DNA Content as a Result of Vigorous Touch Preparations

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1 Original Articles Depletion of Core Needle Biopsy Cellularity and DNA Content as a Result of Vigorous Touch Preparations Natasha Rekhtman, MD, PhD; Sofia Kazi, MD; JinJuan Yao, MD; Snjezana Dogan, MD; Angela Yannes, BS; Oscar Lin, MD, PhD; Mikhail Silk, MD; Tarik Silk, BS; Jeremy C. Durack, MD Context. Touch preparations (TP) of core needle biopsies (CNBs) are used at some institutions for on-site assessment of CNB adequacy. In our clinical practice, we have encountered instances in which TPs resulted in substantial depletion of CNB cellularity. Objective. To examine the effect of increasingly vigorous TPs on cellularity and DNA content of CNBs. Design. Ex vivo CNBs (n ¼ 56) were performed on resected lung and kidney tumor specimens. For each specimen, CNBs were performed in quadruplicate on tumor and nontumor tissue and subjected to 1 of 4 TP methods: imprint, 1-cm drag, 2-cm drag, or full-slide drag. Overall cellularity in TPs relative to corresponding CNBs was estimated semiquantitatively. DNA was extracted and quantified from 12 TPs and corresponding CNBs. Two cytopathologists performed a blinded diagnostic assessment of Diff-Quik stained TPs. Results. Cellularity of imprint, 1-cm, 2-cm, and fullslide TPs represented, on average, 19%, 33%, 41%, and 46% of total CNB cellularity, respectively (P ¼.003). Average DNA content in imprint, 1-cm, and 2-cm TPs was 0.3 lg (range, lg), 0.4 lg (range, lg), and 0.6 lg (range, lg), respectively, which represented on average 15%, 36%, and 50%, respectively, of total CNB DNA content. Diagnostic accuracy was not inferior for less-extensive TPs, compared with more-extensive TPs. Conclusions. Vigorous TPs may contain a substantial fraction of CNB cellularity and DNA content, whereas more-limited TPs are less disruptive to CNBs but remain suitable for cytologic assessment. We suggest avoiding excessively forceful TPs and, whenever clinically feasible, obtaining additional samples to ensure sufficient cellularity for potential ancillary studies. (Arch Pathol Lab Med. 2015;139: ; doi: / arpa oa) During the past decade, computed tomography (CT) guided core needle biopsies (CNBs) and fine-needle aspirates (FNAs) have become the methods of choice for sampling thoracic and abdominal mass-forming lesions, virtually replacing more-invasive surgical procedures. Although imaging provides accurate guidance for needle placement, nondiagnostic specimens may result from sampling of tissue adjacent to the target lesion or sampling of a necrotic or fibrotic area within a tumor. For FNAs, rapid on-site assessment of cytologic smears is a well-established and widely recommended method for assuring adequate lesion sampling; however, there is currently no standard recommendation for on-site assessment of CNBs. Accepted for publication October 27, Published as an Early Online Release December 18, From the Departments of Pathology (Drs Rekhtman, Kazi, Yao, Dogan, and Lin and Ms Yannes); and Radiology (Drs Silk and Durack and Mr Silk), at Memorial Sloan Kettering Cancer Center, New York, New York. Drs Rekhtman and Kazi contributed equally to this manuscript. The authors have no relevant financial interest in the products or companies described in this article. Presented as a platform talk at the annual meeting of the United States and Canadian Academy of Pathology; March 1 7, 2014; San Diego, California. Reprints: Natasha Rekhtman, MD, PhD, Department of Pathology, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY ( rekhtman@mskcc.org). In some institutions, on-site assessment for CNBs is performed via touch preparations (TPs). Touch preparation techniques may vary, but generally involve touching the CNB specimen against a glass slide to create a cytology smear, which is immediately stained and evaluated by a cytotechnologist or cytopathologist, analogous to on-site assessment of FNAs. Most studies on TPs have been based on large-bore breast and bone marrow CNBs, 1 8 and endoscopic gastric mucosal biopsies There have been only a few studies on TPs for CT-guided CNBs, and those studies were focused primarily on the feasibility and the accuracy of cytologic assessment of TPs There are, however, only limited data on the effect of TPs on CNBs. 15,17 A single instance of complete CNB depletion of tumor cells because of TPs has been recorded in the literature, 17 but there has been no quantitative study, to our knowledge, on the overall effect of TPs on CNB cellularity and DNA content. The issue of cell and DNA content in CNBs is increasingly important in current practice, where the availability of material for standard clinical and research protocol ancillary studies, including immunohistochemical, molecular, and cytogenetic, has become essential for the management of many tumor types. At our institution, in the past 3 years, nearly all CT-guided CNBs have been accompanied by on-site assessment by TPs. This practice was initially introduced for research protocols, requiring fresh-frozen CNBs with confirmation that those biopsies contained tumor cells, but it was Arch Pathol Lab Med Vol 139, July 2015 Ex Vivo Touch Preparations Rekhtman et al 907

2 Figure 1. Example of Diff-Quik stained touch preparations. subsequently extended to all CNBs. We noticed considerable variability in CNB cellularity deposited onto TP slides. In addition, we encountered instances, albeit uncommon, in which cellular TPs were associated with minimal or no residual tumor cells in the residual CNBs. This was documented in a recent study 19 from our institution, in which a review of 1100 consecutive CT-guided CNBs revealed that in 15 cases (1.4%), CNBs were substantially or completely depleted (0 20 tumor cells remaining in CNB) as a result of TPs. In another recent clinical series, it was reported that of 140 CT-guided CNBs, tumor exhaustion as a result of TPs occured in 9 (8.2%) of cases. 20 To study these clinical observations in greater detail, we designed an ex vivo study in which we quantitatively evaluated the effect of increasingly vigorous TP on CNB cellularity and DNA content and examined whether more-limited TPs were still sufficient for cytologic evaluation while better preserving CNB cellularity. METHODS This study was performed with approval from the institutional review board of Memorial Sloan Kettering Cancer Center (New York, New York). Ex vivo CNBs (n ¼ 56) were performed on resected lung (n ¼ 4) and kidney (n ¼ 3) specimens after completion of standard dissection and submission of tissue for diagnostic evaluation. Core needle biopsies were performed using 18-gauge side-notch Temno Evolution biopsy needles (CareFusion, San Diego, California), set for 19-mm sampling length (needle maximum); a device commonly used at our institution for CTguided CNBs. For each resection, CNBs were performed in quadruplicate on tumor and nontumor tissue. The CNBs were removed from the core needle side-notch with the aid of a hypodermic needle, and each CNB was subjected to 1 of 4 TP methods: (1) imprint, defined as touching the CNB to the slide with minimal sliding along the slide surface; (2) 1-cm drag, defined as touching the CNB to the slide and sliding it gently along the slide surface with the tip of a needle; (3) 2-cm drag, defined as sliding the CNB for a distance of 2 cm; and (4) full slide drag, defined as sliding the CNB along the full length of the slide. Touch preparations and CNBs were processed by standard procedures: TP slides were air-dried and stained with Diff-Quik (representative example is shown in Figure 1). Core needle biopsies were fixed in 10% neutral-buffered formalin, paraffin-embedded, and step-sectioned at 5-lm intervals until no grossly visible tissue remained in the paraffin block. One section was stained with hematoxylin-eosin and unstained sections were submitted for DNA extraction. Visual assessment of cellularity was performed semiquantitatively by estimating the percentage of overall cellularity of hematoxylin-eosin stained CNB section contained in a Diff- Quik stained TP slide. Because a single hematoxylin-eosin section represents only a fraction of CNB cellularity, we estimated percentages of TP cellularity relative to total CNB by adjusting the counts to the number of levels in an entirely sectioned CNB. Quantitation was performed in triplicate by the same reviewer (S.K.), who was blinded to the results of the previous cell counts, and the average of 3 counts was used for statistical analysis. DNA content was assessed in 12 selected CNBs and corresponding TPs (6 from tumor and 6 from benign tissue); selection was based on chronologic order of sample procurement. DNA extraction from scraped TPs and paraffin-embedded sections was performed following the standard protocol in Memorial Sloan Kettering Cancer Center Diagnostic Molecular Pathology Laboratory. DNA was extracted using the DNeasy blood and tissue kit (Qiagen, Valencia, California) and eluted in 50-lL of Tris-EDTA buffer. DNA concentration was measured using a Qubit Fluorometer (Life Technologies, Carlsbad, California). DNA content was calculated by multiplying DNA concentration by elution volume. Total (pre-tp) DNA content of CNB was calculated by summing DNA content in post-tp CNB and DNA content in the corresponding TP. For the blinded diagnostic assessment, Diff-Quik stained TPs from tumor and nontumor tissue were randomized and distributed to 2 cytopathologists (N.R. and O.L.). Each TP was categorized as lesional, nonlesional, or defer. The reviewers were asked to document whether the slide review was subjectively difficult (yes or no), defined as having to review the slide more than once before rendering a diagnosis. Reviewers were also asked to record whether having a sample with greater cellularity was desirable (yes or no). Diagnostic accuracy, subjective difficulty, and subjective impression of limited cellularity were compared for the 4 TP methods. RESULTS Quantitation of cellularity in 56 paired TPs and corresponding CNBs is shown in Figure 2. On average, imprint, 1-cm drag, 2-cm drag, and full-slide drag contained the following fraction of total CNB cellularity: 19% (range, 8% 49%), 33% (range, 15% 72%), 41% (range, 18% 82%), and 46% (range, 17% 90%), respectively (Figure 2, A). Although there was a substantial range of cellularity deposited onto TP slides prepared with each method, greater depletion of CNBs with more extensive TPs was statistically significant (P ¼.003; 1-way analysis of variance). We did not identify complete cellular depletion for any CNBs, but the loss of cellularity reached up to 90% with some full-slide TPs. Tumors showed a significantly greater loss of cellularity than 908 Arch Pathol Lab Med Vol 139, July 2015 Ex Vivo Touch Preparations Rekhtman et al

3 Figure 2. Quantitation of cellularity in touch preparations (TPs) and corresponding core needle biopsies (CNBs). A, Percentage of CNB cellularity lost into TPs for each TP method. Each bar represents mean and standard deviation for 14 CNB/TP pairs. B, Percentage of CNB cellularity lost into TPs for tumor versus benign tissue. Each bar represents mean and standard deviation for 28 CNB/TP pairs. benign tissue (mean [SD], 43% [22%] versus 27% [16%], respectively; P ¼.003; unpaired t test) (Figure 2, B). Findings were comparable for kidney and lung specimens analyzed separately. DNA content in 12 CNBs and corresponding TPs is shown in Figure 3. Average DNA content in imprint, 1-cm drag, and 2-cm drag was 0.3 lg (range, lg), 0.4 lg (range, lg), and 0.6 lg (range, lg), respectively (Figure 3, A), whereas average DNA content in corresponding CNBs was 1.7 lg (range, lg), 0.7 lg (range, lg), and 0.6 lg (range, lg), respectively (Figure 3B). DNA content in imprint, 1-cm drag, and 2-cm drag represented on average 15%, 36%, and 50% of total CNB DNA content, respectively (Figure 3, C). Differences in DNA content between TP methods did not reach statistical significance, likely because of the few tested samples. Blinded cytologic assessment of TPs by 2 cytopathologists is shown in the Table. Combined data for the 2 pathologists (102 total cytologic assessments; 28 assessment per each TP type) showed that misclassified/deferred diagnoses were distributed as follows: imprint (n ¼ 2; 7%), 1-cm drag (none; 0%), 2-cm drag (none; 0%), and full-slide drag (n ¼ 2; 7%). Touch preparations marked as difficult included imprint (n ¼ 1; 3.5%) and full-slide drag (n ¼ 1; 3.5%), and more material desirable included imprints (n ¼ 2; 7%), 2-cm drag (n ¼ 1; 3.5%), and full-slide drag (n ¼ 2; 7%). Overall, all types of TP preparations were comparable for cytologic assessment. Figure 3. DNA content in touch preparations (TPs) and corresponding core needle biopsies (CNBs). Shown is mean and standard deviation for DNA content in (A) TPs (n ¼ 4) and (B) CNBs (n ¼ 4), and (C) the percentage of total CNB DNA content lost into TPs (each bar, n ¼ 4 paired samples). Three of 4 incorrect/deferred interpretations (75%) of TPs were attributable to a single lung specimen, in which benign tissue contained abundant megakaryocytes an enigmatic but well-documented finding in lung specimens, 21 which mimicked lesional tissue in smears with both lower and higher cellularity. The interpretation of megakaryocytes in benign lung also accounted for the only imprint that was reported as difficult. COMMENT In this ex vivo study, we found that extensive TPs can substantially reduce CNB cellularity and DNA content, whereas more-limited TPs are less depleting to CNBs but Arch Pathol Lab Med Vol 139, July 2015 Ex Vivo Touch Preparations Rekhtman et al 909

4 TP Type Blinded Cytologic Assessment of Touch Preparations (TPs) for Core Needle Biopsies of Tumor and Nontumor Tissue Pathologist 1, Wrong/Deferred Difficult More Material Desirable Pathologist 2, Pathologist 1, Pathologist 2, Pathologist 1, Pathologist 2, Imprint, n ¼ 14 1 (7) 1 (7) 1 (7) 0 2 (14) 0 1 cm, n ¼ cm, n ¼ (7) 0 Full slide, n ¼ (14) 0 1 (7) 1 (7) 1 (7) are still suitable for cytologic assessment. These findings model our observations from clinical practice, in which some TPs resulted in marked or complete depletion of CNB cellularity an issue that has only recently come to attention in the literature. 19,20 Our finding regarding the risk of CNB depletion from TPs must be viewed in the context of the overall clinical benefit of this practice. The practice of performing TPs on CTguided CNBs is relatively new, and to our knowledge, no formal study has evaluated the overall clinical benefit of its routine use relative to CNBs with no on-site assessment or with more traditional on-site assessment performed on concurrent FNA. For FNAs, it is well established that on-site assessment offers a substantial clinical benefit by reducing the rate of nondiagnostic specimens by 12% to 22% In addition to gaining immediate knowledge regarding targeting accuracy, on-site assessment affords the ability to triage fresh tissue for ancillary studies, such as microbiologic cultures or flow cytometry. Similar clinical benefit can be expected for on-site assessment of CNBs. Thus, TPs represent a double-edge sword for CNB evaluation on the one hand, they ensure that the target lesion has been sampled, but on the other hand, they introduce the risk of the CNB being depleted of diagnostic cells. Although the focus of this study is on CNBs, similar considerations apply to on-site assessment of FNAs, in that cellularity used up for smears subtracts from the cellularity that can be captured in a cell block and used subsequently for ancillary studies. Our findings suggest that CNB depletion may be ameliorated by avoiding excessively vigorous TPs and, instead, performing light imprints or limited drags. However, we also found that even some imprints caused nonnegligible (up to 50%) cell transfer onto TP slides. This may be related to inherent tissue properties, such that more discohesive or friable tumors result in greater cell transfer even with light TPs, particularly if tumor is present primarily at the edge of the CNB. The role of tissue properties in the differential adherence of cells to a slide surface is supported by our finding that tumors release greater cellularity onto TP slides than do benign tissues, as also recently demonstrated by Dogan et al 26 for imprints on resected tumors. In addition, CNB fragmentation may occur because of even gentle manipulation on the slide surface, resulting in the loss of small fragments. Thus, whenever TP is performed in clinical practice, even if limited in extent, there is a potential possibility of substantial loss of diagnostic material. To make a provision for this possibility, we suggest that whenever clinically feasible, additional samples CNBs and/or FNAs should be routinely procured once targeting accuracy is confirmed through on-site assessment. This is particularly important in the organ systems, such as lung, where the amount of tissue in small specimens is a critical consideration given the routine requirement for ancillary molecular studies to guide targeted therapy. The flip side of the recommendation to limit the extent of TPs is the concern that insufficient cell transfer onto TP slide will result in a false-negative cytologic assessment. Although even the most limited TPs (imprints) on ex vivo CNBs in this study were sufficiently cellular for cytologic assessment, as discussed below, it is possible that some in vivo CNBs may be more admixed with blood than ex vivo CNBs, reducing the surface tension with the slide surface and decreasing cell transfer. In fact, a limited trial of imprints on in vivo CNBs at our institution yielded unsatisfactory results because of the insufficient cellularity of TPs (J.C.D., unpublished data). Thus, there may be a reasonable concern that some in vivo imprints would be too sparse for cytologic assessment. As a practical compromise between preserving cellularity in CNBs and allowing enough cell transfer for on-site assessment, we suggest that optimal TP extent may consist of a short, gentle CNB drag for a distance not exceeding 1 cm, but this suggestion needs further in vivo validation. In prior publications, 2 types of TP techniques on CNBs have been described. One technique is similar to the one used in this study, in which CNB is removed from the needle and moved along the slide surface; this technique is alternatively called core roll preparation. 15,17 The second method, described in Hahn et al 16 and Jacobson et al, 17 involves performing TPs while keeping the CNB inside the needle, exposed to the slide through the window of the side-notch opening. In preliminary studies, we attempted the latter method, but were unable to obtain adequate TPs because the walls of the needle surrounding the exposed CNB prevented the contact between CNB and the slide surface. This difference with prior studies may be related to the use of needles from different manufacturers. In theory, a potential solution for a case requiring ancillary studies in which CNB was depleted could be to sacrifice a TP slide for those studies. Indeed, it is well established that cytologic smears represent an excellent source of material for molecular and cytogenetic analyses However, some tumors require multimodality testing, which, in the case of lung adenocarcinoma, routinely include immunohistochemistry for tumor subtyping, molecular studies for EGFR mutations, and cytogenetic studies for ALK rearrangements. 30 Complete testing of this type would not be feasible using a single smear, even if highly cellular, in most pathology laboratories. Furthermore, sacrificing the sole diagnostic material conflicts with current regulations on retention of diagnostic slides in some states, although the College of American Pathologists has recently updated its guidelines to indicate that laboratories may utilize archived slides for the benefit of the patient, even if that use destroys the slide. 31 Overall, even though partial testing may be 910 Arch Pathol Lab Med Vol 139, July 2015 Ex Vivo Touch Preparations Rekhtman et al

5 possible on a TP slide, to ensure feasibility of a complete ancillary work-up, it is important to avoid cases consisting of a single, positive smear and a depleted CNB, which, as discussed above, can be achieved by (1) limiting the extent of TPs, and (2) avoiding single-pass procedures, if clinically feasible. It is important to note that minimizing the loss of cellularity from CNBs during on-site assessment is only one measure toward increasing sufficiency of CNBs for molecular studies. Other factors can affect the quality and quantity of CNB material, including intraoperative factors, such as the type and location of the target lesion, and the number and type of needle passes. In addition, tissue handling in pathology laboratories should be optimized to maximally preserve tissue in small samples, which may be achieved through separate embedding of multiple CNBs, minimizing the number of initial hematoxylin-eosin sections, using minimal but efficient immunohistochemical panels and minimizing the number of sequential times the block is faced, as reviewed in Travis and Rekhtman. 32 Lastly, sufficiency of small samples is highly dependent on the sensitivity of molecular methods. Thus, maximizing small specimen sufficiency for molecular studies requires a multidisciplinary effort, with optimization of various steps along the entire process, in the context of maintaining patient safety and diagnostic accuracy. Although not the focus of this study, TPs present several other challenges to pathology laboratories. In particular, although on-site assessment is provided by cytopathologists or cytotechnologists, in subspecialized practices, CNBs are frequently signed out by surgical pathologists, creating specimen workflow quandaries. Ideally, CNB and TP should be reviewed by the same pathologist, such that final diagnosis can incorporate the findings from both specimens, and any discrepancies can be reconciled prospectively, as in situations where the CNB is depleted, and all tumor cells are contained in a TP slide. The other challenge with immediate cytologic evaluation of TPs, which similarly applies to onsite assessment for FNAs, is inadequate reimbursement. 33 This study has several limitations. First, because it was an ex vivo study, the specimens examined here may differ in some respects from clinical CNBs and TPs. In particular, in the absence of active blood flow, ex vivo CNBs are only minimally admixed with blood, which, in some cases, may have resulted in greater surface tension between CNBs and the slide surface and exaggerated transfer of cells into TP smears, compared with in vivo specimens, as discussed above. Second, all CNBs in this study were procured with an 18-gauge needle, whereas other needle sizes are employed in clinical practice and may have different propensity for depletion by TPs, as suggested in our clinical study where smaller-gauge CNBs were associated with more-frequent depletion. 19 Third, in this study, we modeled an idealized diagnostic assessment, because CNBs were derived from clear areas of tumor or benign tissue. Clinical CNBs, in contrast, may sample the edge of a tumor and/or contain benign tissue picked up en route to the lesion and can, therefore, contain a mixture of neoplastic and nonneoplastic elements, making the interpretation of corresponding TPs more difficult. Our findings suggest that, at least in some cases, difficulty with the diagnostic assessment is related to the nature of the target tissue, which can present similar difficulty in smears of both lower and higher cellularity. However, we acknowledge that, in some instances, difficult lesions may be more amenable to interpretation when represented with greater cellularity. CONCLUSIONS In this ex vivo study, we have modeled depletion of CNB cellularity and DNA content as a result of extensive TPs. Based on our findings, we suggest avoiding excessively vigorous TPs and, whenever clinically feasible, routinely obtaining additional CNBs and/or FNAs once targeting accuracy is confirmed through on-site assessment to ensure sufficient cellularity for potential ancillary studies, particularly in organs were molecular testing is the standard of care. References 1. Albert US, Duda V, Hadji P, et al. Imprint cytology of core needle biopsy specimens of breast lesions: a rapid approach to detecting malignancies, with comparison of cytologic and histopathologic analyses of 173 cases. Acta Cytol. 2000;44(1): Carmichael AR, Berresford A, Sami A, Boparai R. Imprint cytology of needle core-biopsy specimens of breast lesion: is it best of both worlds? Breast. 2004;13(3): Crisan D, Farkas DH. Bone marrow biopsy imprint preparations: use for molecular diagnostics in leukemias. Ann Clin Lab Sci. 1993;23(6): Green RS, Mathew S. 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6 patients and metaanalysis of the literature. AJR Am J Roentgenol. 1993;160(1): Nasuti JF, Gupta PK, Baloch ZW. Diagnostic value and cost-effectiveness of on-site evaluation of fine-needle aspiration specimens: review of 5688 cases. Diagn Cytopathol. 2002;27(1): Saleh HA, Khatib G. Positive economic and diagnostic accuracy impacts of on-site evaluation of fine needle aspiration biopsies by pathologists. Acta Cytol. 1996;40(6): Santambrogio L, Nosotti M, Bellaviti N, Pavoni G, Radice F, Caputo V. CTguided fine-needle aspiration cytology of solitary pulmonary nodules: a prospective, randomized study of immediate cytologic evaluation. Chest. 1997; 112(2): Dogan S, Becker JC, Rekhtman N, et al. Use of touch imprint cytology as a simple method to enrich tumor cells for molecular analysis. Cancer Cytopathol. 2013;121(7): Aisner DL, Sams SB. The role of cytology specimens in molecular testing of solid tumors: techniques, limitations, and opportunities. Diagn Cytopathol. 2012; 40(6): Savic S, Bubendorf L. Role of fluorescence in situ hybridization in lung cancer cytology. Acta Cytol. 2012;56(6): Knoepp SM, Roh MH. Ancillary techniques on direct-smear aspirate slides: a significant evolution for cytopathology techniques. Cancer Cytopathol. 2013; 121(3): Lindeman NI, Cagle PT, Beasley MB, et al. Molecular testing guideline for selection of lung cancer patients for EGFR and ALK tyrosine kinase inhibitors: guideline from the College of American Pathologists, International Association for the Study of Lung Cancer, and Association for Molecular Pathology. Arch Pathol Lab Med. 2013;137(6): College of American Pathologists. CAP Laboratory Cytopathology accreditation checklists CYP Slide Retention Phase II. cap.org. Accessed April 21, Travis WD, Rekhtman N. Pathological diagnosis and classification of lung cancer in small biopsies and cytology: strategic management of tissue for molecular testing. Semin Respir Crit Care Med. 2011;32(1): Dhillon I, Pitman MB, Demay RM, Archuletta P, Shidham VB. Compensation crisis related to the onsite adequacy evaluation during FNA procedures-urgent proactive input from cytopathology community is critical to establish appropriate reimbursement for CPT code (or its new counterpart if introduced in the future). Cytojournal. 2010;7:23. doi: / Arch Pathol Lab Med Vol 139, July 2015 Ex Vivo Touch Preparations Rekhtman et al

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