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Journal of Oncology Practice logoLink to Journal of Oncology Practice
. 2018 Oct 4;14(11):e722–e728. doi: 10.1200/JOP.18.00092

What Can Be Done to Improve Research Biopsy Quality in Oncology Clinical Trials?

Katherine V Ferry-Galow 1, Vivekananda Datta 1, Hala R Makhlouf 1, John Wright 1, Bradford J Wood 1, Elliot Levy 1, Etta D Pisano 1, Alda L Tam 1, Susanna I Lee 1, Umar Mahmood 1, Lawrence V Rubinstein 1, James H Doroshow 1, Alice P Chen 1,✉
PMCID: PMC6237512  PMID: 30285529

Abstract

Purpose:

Research biopsy specimens collected in clinical trials often present requirements beyond those of tumor biopsy specimens collected for diagnostic purposes. Research biopsies underpin hypothesis-driven drug development, pharmacodynamic assessment of molecularly targeted anticancer agents, and, increasingly, genomic assessment for precision medicine; insufficient biopsy specimen quality or quantity therefore compromises the scientific value of a study and the resources devoted to it, as well as each patient’s contribution to and potential benefit from a clinical trial.

Methods:

To improve research biopsy specimen quality, we consulted with other translational oncology teams and reviewed current best practices.

Results:

Among the recommendations were improving communication between oncologists and interventional radiologists, providing feedback on specimen sufficiency, increasing academic recognition and financial support for the time investment required by radiologists to collect and preserve research biopsy specimens, and improving real-time assessment of tissue quality.

Conclusion:

Implementing these recommendations at the National Cancer Institute’s Developmental Therapeutics Clinic has demonstrably improved the quality of biopsy specimens collected; more widespread dissemination of these recommendations beyond large clinical cancer centers is possible and will be of value to the community in improving clinical research and, ultimately, patient care.

INTRODUCTION

Clinical trials with pharmacodynamic study objectives routinely require that patients undergo one or more image-guided tumor biopsies to participate; trial success depends on the quality of the tumor samples obtained. A retrospective analysis of research biopsy tissues obtained in four early-phase clinical trials at the National Cancer Institute (NCI) Developmental Therapeutics Clinic found that only 83 of 112 18-gauge needle biopsies performed for pharmacodynamic studies using slide-based analyses (74%) met assay quality control criteria; reasons for failure included extensive necrosis or fibrosis, no or insufficient tumor content, and/or inadequate tissue quality for morphologic assessment.1,2 The most common reason for failure was the absence of tumor (Fig 1); 44% of the biopsy specimens evaluated contained < 25% viable tumor cells, rates comparable to those reported at other clinical centers.3 These insufficiency rates are somewhat higher than those previously cited for diagnostic biopsies3-6 because of the greater amount of tumor and control of preanalytical variables required for successful pharmacodynamic analyses. When both pre- and post-treatment (paired) biopsy specimens are required to measure pharmacologic modulation of a specific drug target, only approximately 50% of patients had sufficient paired tissue collected for analysis. For clinical trial design, this 50% failure rate requires performing paired biopsies on 15 patients for an 85% likelihood of having at least six usable paired samples. Even when biopsy specimens of sufficient tumor content are collected, the implementation of analyte-specific collection methods can be logistically challenging. For example, handling time is critical if the target molecule undergoes degradation during processing (eg, molecules in hypoxia- or phosphorylation-related pathways).7,8 Sample preparation depends on tissue use: whole-biopsy extraction assays often require specimens to be flash frozen and then homogenized,7-11 whereas slide-based analyses require frozen cores to be formalin fixed and paraffin embedded for sectioning.12

Fig 1.

Fig 1.

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Insufficient tumor content is a primary cause of biopsy specimen inadequacy; collecting multiple cores from each patient during each needle biopsy procedure increases the likelihood of obtaining sufficient paired biopsy samples for pharmacodynamic analysis. At the NCI Developmental Therapeutics Clinic, hematoxylin and eosin–stained slides are prepared for evaluation of viable biopsy tumor content and quality by an anatomic pathologist. Sections of (A) the first core and (B) the second core from a patient with cholangiocarcinoma during the same liver biopsy procedure are shown; the relative tumor contents are < 5% and > 50%, respectively. Green boxes indicate tumor area.

Inadequate biopsy tumor content is also a barrier to precision medicine clinical trials in which genetic sequencing establishes trial eligibility or influences treatment selection. Protocols involving next-generation sequencing assays, for example, often require tumor enrichment if the proportion of tumor in the biopsy decreases below a certain percentage necessary to obtain a sufficient quantity of high-quality nucleic acid, thus delaying the next-generation sequencing results and any dependent treatment decisions. Although liquid biopsies (ie, circulating cell-free DNA analysis) hold promise for identification of tumor genetic abnormalities,13 they cannot reveal tumor heterogeneity or the cellular source of a signal, making tumor biopsy the gold standard sampling modality for both genetic and pharmacodynamic analyses.

METHODS

Community Discussion of Best Practices

To gain an understanding of how the wider oncology research community was addressing these issues, the NCI convened three national meetings with medical oncologists, diagnostic and interventional radiologists, and pathologists to review current practices and to identify measures that could improve the quality of research biopsy specimens in clinical trials. Recommendations on how to improve biopsy quality were compiled from meeting presentations and participant discussions (Box 1). The major concerns of participants included a lack of broad recognition of the differential requirements for diagnostic and research biopsy specimens, an absence of communication between oncologists and interventional radiologists regarding the rationale for obtaining research biopsy specimens that contain tumor tissue adequate for research objectives, and insufficient academic recognition and financial support for the greater time investment required to collect research biopsy specimens.

Box 1. Critical Recommendations to Improve the Quality of Research Biopsy Specimens in Cancer Clinical Trials

  • Include on the research team interventional radiologists who will perform research biopsies.

  • Facilitate better communication among diagnostic radiologists, interventional radiologists, medical oncologists, pathologists, and laboratory researchers during clinical protocol development to establish research needs (eg, No. of tumor cores required, preferred tumor region to be sampled, and so forth) and at designated time points during the trial to assess and discuss success rates and research outcomes.

  • Obtain informed consent to collect up to five cores per biopsy procedure if safe and feasible.

  • Create protocol-specific standard operating procedures or appendices that detail research biopsy specimen quality requirements for the selected assay, such as No. of cores needed, fixation method for each core, and any requirements for the tumor region from which the biopsy specimen should be collected, to guide the radiologist and help ensure that requirements and expectations (of the researcher, radiologist, and patient) are met.

  • Review each patient with interventional radiologist to ensure that patients who do not have tumors amenable to biopsy are not enrolled in a clinical trial with a research biopsy requirement. A prescreening scoring system that is based on the presence of a lesion suitable for biopsy, whether the selected lesion can be sampled aggressively, and the expected level of risk of major complication, will help assess the likelihood that a target lesion will yield sufficient material.14-16

  • Prepare evidence-based practice guidelines for biopsy methodology and other materials that convey the added value from collaborative efforts to collect better biopsy samples. This may help administrative staff and others in resource assignment roles develop a reimbursement plan for research tissue sampling that reflects the extra time and imaging methodologies needed for the biopsy team to obtain better tumor biopsy samples.

One critical point is that the traditional goal of interventional radiologists has been to obtain the minimum tissue needed for histologic diagnosis to optimize patient safety, but in the research setting, radiologists are increasingly asked to obtain sufficient tissue for genomic and/or pharmacodynamic assessment. As gatekeepers tasked with evaluating patient risk relative to potential research reward, radiologists are responsible for selecting a target lesion, judging how many needle biopsy cores can be collected safely, evaluating and treating patient discomfort, selecting the biopsy tools and imaging modality for guidance, adjusting the procedure on the basis of real-time imaging and tissue adequacy information, and addressing any complications. Although protocols generally include specific requirements for sample collection and processing, these requirements are not always conveyed to those performing biopsy procedures. In the absence of a description of the trial’s scientific and medical goals and clear directions about sample requirements, a radiologist may justifiably stop the procedure prematurely to minimize possible complications. There are no established guidelines for a maximum number of core specimens, but participants reported obtaining three to six cores per procedure for research purposes and agreed that research biopsy collection was safe relative to biopsies performed for medical reasons.17,18 Meeting participants agreed that implementation of a prebiopsy scoring system, such as that implemented at MD Anderson Cancer Center to assess the likelihood that a target lesion will yield sufficient material for molecular testing, would contribute to significant improvement in the rate of successful research biopsy specimens. The three main factors considered in the MD Anderson system are (1) whether a suitable lesion (viable tumor) for biopsy is present; (2) whether the lesion selected for biopsy can be sampled aggressively; and (3) the expected level of risk of major complication. The outcome of such prescreening may be to identify and exclude from enrollment those patients whose tumors are least likely to provide biopsy specimens sufficient for research.14

Tracking and Assessing Tumor Biopsy Quality

Assessment of hematoxylin and eosin–stained slides by an anatomic pathologist before analysis of formalin-fixed, paraffin-embedded sections in slide-based pharmacodynamic assays initially revealed a high rate of biopsy specimens insufficient for the intended analysis. As part of a due diligence effort to investigate the root cause of the failures, NCI’s Developmental Therapeutics Program, in collaboration with the pharmacodynamic assay group, established a defined scoring system to standardize assessment of specimen sufficiency to facilitate clear feedback to the clinical team. Biopsy specimens were rated for viable tumor content according to the following four categories: > 50% (optimal), 25% to 50% (acceptable), 5% to 25% (low tumor content), and < 5% (unanalyzable). Using advanced image analysis methods, biopsy specimens with low tumor content (5% to 25% viable tumor content) are considered analyzable in slide-based analyses but inadequate for whole-biopsy extraction–based analyses because there is currently no validated method to normalize the tumor content. Biopsy specimens containing < 5% viable tumor are considered unsuitable for any pharmacodynamic assay format because not enough tumor cells are present to adequately assess biomarker response. Also as a result of this due diligence effort, a biopsy team composed of radiologists, oncologists, pathologists, and assay scientists was established to regularly communicate regarding the purpose, requirements, collection parameters and resulting quality of each biopsy, with the aim of identifying aspects of lesion selection, imaging modality choice, and collection technique that correlate with tissue quality and intended use.

RESULTS

Encouraging Communication and Collaboration

Careful tracking of tumor biopsy specimen sufficiency demonstrated that only 74% of biopsy specimens (83 of 112) collected for research purposes at the NCI Developmental Therapeutics Clinic were sufficient for slide-based pharmacodynamic assessments at the outset of this analysis. Once the scale of the problem became clear, the first course of action at the clinic was to establish early and consistent communication with the interventional radiologists performing the biopsy procedures. Providing interventional radiologists with more information about protocol research goals and sample requirements allows them to collect the best biopsy specimens from each patient as circumstances allow. Inviting the radiologists to join the research team, review the protocol, and participate in meetings to discuss the success and failure rates of research biopsy specimens has favorably affected biopsy efficiency and workflow. Radiologists can in turn provide guidance and integrate information derived from their technical skill and experience, such as intentionally sampling from the invasive front of the tumor (for studies of tumor microenvironment effects on metastasis) or regions of hypervascularity (for antivascular agents) or of high 18F-fluorodeoxyglucose avidity to inform the research objectives. Wherever possible, the radiology team captures images documenting biopsy needle placement that can be reviewed together with tumor biopsy quality data to assess imaging characteristics that may inform viable tumor zones. These interactions require an investment of time for which they are inadequately compensated, as noted by meeting participants. The challenges of having these efforts recognized at a large research-directed cancer center may be different from those at a smaller community site, but communicating the added value from the collaboration to appropriate administrative staff, with the goal of promoting recognition of the effort, is a major objective of this NCI biopsy quality initiative.

Protocol pharmacodynamic objectives may call for collecting a post-treatment biopsy specimen from the same lesion or location as the initial biopsy to minimize tissue heterogeneity caused by different tumor microenvironments, but the radiologist has the discretion to biopsy different lesions to avoid sample degradation related to fibrosis artifacts that may arise from resampling recently biopsied tissue.19,20 Adequately weighing such considerations cannot be accomplished with a one-time biopsy order; it is a process requiring ongoing communication. In this case, documentation of biopsy site adds additional research value by enhancing the ability of oncologists to monitor the response(s) of specific lesions that were biopsied in conjunction with Response Evaluation Criteria in Solid Tumors (RECIST) monitoring for patient response.21

Collection of Multiple Tissue Cores

Knowing the requirements and planned use for biopsy tissue in a trial also guides the radiologist when deciding whether to collect multiple cores during each image-guided procedure if safe and feasible,18 particularly when biopsy-derived data are used for clinical decision making. For example, in the NCI MPACT study (Molecular Profiling-based Assignment of Cancer Therapy for Patients With Advanced Solid Tumors; ClinicalTrials.gov identifier: NCT01827384),22,23 ≥ 50% tumor content is generally required to generate the integral genetic sequencing data used to direct treatment selection without additional tumor enrichment. Of 187 biopsy cores received from the first 93 patients enrolled in this trial, 112 cores (60%) met this ≥ 50% tumor content criterion, whereas 53 cores (28%) contained < 50% tumor, and 22 cores (12%) contained no tumor cells. Collecting just two cores per biopsy procedure provided sufficient DNA for sequencing all but five patients (5%). Successful pharmacodynamic analyses of biopsy pairs have been performed with tumor content as low as 5% by applying a tumor marker mask, whereas a minimum of 25% tumor is considered adequate for a reliable whole-biopsy, extraction-based analysis. For recent slide-based pharmacodynamic analyses at the NCI Developmental Therapeutics Clinic, allowing collection of up to five cores per biopsy procedure if needed (on average, only three cores are actually collected), together with improved communication with the radiology team and an improved imaging process allowing for the analysis of tissues with lower tumor content, has increased the likelihood of obtaining sufficient paired pharmacodynamic samples from 50% to > 80%.

DISCUSSION

Collecting research tumor biopsy specimens that are fit-for-purpose for pharmacodynamic or predictive biomarker assays presents challenges, but immediate improvements in biopsy specimen quality are possible through simple changes such as early and consistent communication with the interventional radiologists about protocol design and research objectives. Some improvements may be limited to specialized cancer centers. For example, wherever possible, the NIH Clinical Center radiology team captures images documenting biopsy needle placement that can be reviewed together with tumor biopsy quality data to assess imaging characteristics that inform viable tumor zones. New, minimally invasive technologies to visualize the tumor in situ, such as smart spectroscopic needles that use optical imaging to verify needle location24,25 or techniques such as magnetic resonance and ultrasound fusion,26 may in the future improve tissue targeting. Likewise, in-suite cytopathology review procedures at the time of biopsy core collection, such as touch preps and initial fine-needle aspirates to identify tumor-enriched zones, can prompt additional tissue collection when initial samples are inadequate, but they obviously require additional staff and resources. Other, more readily achievable procedural changes, such as including those who perform biopsies as associate investigators in clinical protocols and as authors on clinical manuscripts, serve to document the contribution of time, effort, and technical expertise and may provide grounds for increased compensation under various reimbursement systems such as grants and insurance. Perhaps the most surprising finding from our meetings with interventional radiologists was the number who were unaware that their biopsy samples were so often not fit for purpose. They often are unaware of the purpose of the biopsy (ie, research v diagnosis) or whether specific tumor regions or numbers of cores were needed, and they received no feedback on quality. Improving this cross-discipline communication and collaboration is a remedy available to all types of care settings.

Collecting multiple cores for research is another highly effective strategy and will be influenced by the need to minimize patient inconvenience and risk. Moreover, the requirement for multiple biopsy procedures for individual patients in some trials and the increasing interest in collecting tissue for biobanking may compete with the goals of biomarker investigations,1,27-29 an issue that can be addressed partially by incorporating a formal biopsy tissue allocation plan into each clinical protocol. It is worth emphasizing that, for pharmacodynamic-driven trials, a slight increase in the number of cores collected per procedure may decrease the total number of patients needed to meet trial objectives and maximize the research knowledge obtained from all subjects.

The meetings held with the oncology research community marshalled enthusiasm to communicate the need and resources available for improving research biopsy specimen quality. The NCI Division of Cancer Treatment and Diagnosis posts standard operating procedures for tissue collection on its website for validated biomarker assays,30 and the publicly available Biospecimen Research Database31 infrastructure is being revised as a resource to promote the dissemination of pathology-radiology references, data, and best practices. Additional outreach at national meetings and through professional societies is planned to raise awareness and to publicize the financial support available for this critical area of research.

ACKNOWLEDGMENT

Supported in whole or in part with federal funds from the National Cancer Institute, National Institutes of Health (NIH), under Contract No. HHSN261200800001E. Supported in part by the Intramural Research Program of the NIH and the NIH Center for Interventional Oncology. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government. We thank Ralph E. Parchment, PhD, Leidos Biomedical Research, for his insightful comments, Andrea Regier Voth, PhD, Leidos Biomedical Research, for editing and writing support, and Karen Gray, PhD, Leidos Biomedical Research, for organizing the meetings.

AUTHOR CONTRIBUTIONS

Conception and design: Katherine V. Ferry-Galow, Vivekananda Datta, Hala R. Makhlouf, Bradford J. Wood, Etta D. Pisano, Alda L. Tam, Susanna I. Lee, Umar Mahmood, James H. Doroshow

Financial support: James H. Doroshow

Administrative support: John Wright, James H. Doroshow

Provision of study material or patients: Bradford J. Wood, James H. Doroshow

Collection and assembly of data: Katherine V. Ferry-Galow, Vivekananda Datta, Hala R. Makhlouf, Bradford J. Wood, Alda L. Tam, Alice P. Chen

Data analysis and interpretation: Katherine V. Ferry-Galow, Vivekananda Datta, Hala R. Makhlouf, John Wright, Bradford J. Wood, Elliot Levy, Alda L. Tam, Susanna I. Lee, Lawrence V. Rubinstein, James H. Doroshow, Alice P. Chen

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

What Can Be Done to Improve Research Biopsy Quality in Oncology Clinical Trials?

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/jop/site/ifc/journal-policies.html.

Katherine V. Ferry-Galow

Stock and Other Ownership Interests: Johnson & Johnson

Vivekananda Datta

No relationship to disclose

Hala R. Makhlouf

No relationship to disclose

John Wright

No relationship to disclose

Bradford J. Wood

Research Funding: Philips Healthcare (Inst), Philips/inVivo (Inst), Biocompatibles (Inst), Celsion Corp (Inst), Xanthus (Inst), Siemens (Inst), Navidea (Inst)

Patents, Royalties, Other Intellectual Property: NIH and Philips have a licensed shared patents and intellectual property, under which I receive royalties; NIH and Biocompatibles share intellectual property and patents in the field of drug eluting microspheres for tumor embolization (Inst); named as inventor on multiple patents, invention reports, and intellectual property (Inst).

Travel, Accommodations, Expenses: Philips Healthcare, Biocompatibles, Xanthus, Siemens, Navidea

Other Relationship: Springer, Smart Cities Media

Elliot Levy

Stock and Other Ownership Interests: Halyard Health

Etta D. Pisano

Research Funding: Freenome Holdings I c; Therapixel, Koning, Philips Healthcare

Patents, Royalties, Other Intellectual Property: I have several patents, none of which have paid me any royalties.

Alda L. Tam

Honoraria: Merit Medical Systems, Galil Medical

Consulting or Advisory Role: Abbvie, Jounce Therapeutics, Siemens

Research Funding: AngioDynamics, Guerbet

Travel, Accommodations, Expenses: Guerbet

Susanna I. Lee

Employment: UpToDate

Umar Mahmood

Leadership: CytoSite Biopharma

Stock and Other Ownership Interests: CytoSite Biopharma

Consulting or Advisory Role: CytoSite Biopharma

Patents, Royalties, Other Intellectual Property: Patents related to granzyme B imaging and therapy.

Lawrence V. Rubinstein

No relationship to disclose

James H. Doroshow

No relationship to disclose

Alice P. Chen

No relationship to disclose

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