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SIXTEENTH ANNUAL WARREN K. SINCLAIR KEYNOTE ADDRESS:


FRONTIERS IN MEDICAL RADIATION SCIENCE

C. Norman Coleman1,2

2018), radiation medicine (Brink 2008; Mettler et al. 2013;


Abstract—On the occasion of the 90th anniversary of National Coun-
cil on Radiation Protection and Measurements (NCRP) and its 55th Rosenstein 2019), and “Where are the Radiation Profes-
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anniversary since being Congressionally Chartered, the theme of sionals?” (Bushberg 2015; Toohey 2017). The varied and
“Providing Best Answers to Your Most Pressing Questions about timely topics are a credit to Warren Sinclair in recognition
Radiation” is most appropriate. The question proposed here is, of his service to the National Council on Radiation Protection
“What are the new frontiers for the NCRP with its breadth of talent
and expertise in the rapidly evolving era of precision medicine?” and Measurements (NCRP) and its vision for the future.
Three closely related themes are presented for new applications of This meeting marks the transition of presidents of the
radiation science for research and career opportunities: (1) intro- NCRP between two colleagues of mine. These professional
duction of the new concept of defining radiation dose in biological relationships go back first to the 1980s when I was at Stanford
perturbations in addition to physical dose, particularly for cancer
treatment; (2) assessment of early biomarkers of radiation injury studying secondary cancers in patients treated for Hodgkin’s
for mass casualty exposure (biodosimetry) to guide triage and for disease, at which time I learned a great deal from the ep-
clinical application to guide radiation therapy; and (3) proposal idemiology work of John Boice, who was at the National
to expand opportunities for radiation professionals, including Cancer Institute (NCI) and from one of his students who
consideration of a new training program within NCRP’s “Where
are the radiation professionals?” initiative that trains radiation became my colleague at Stanford, Peggy Tucker; and sec-
oncologists as molecular radiation epidemiologists. ond to the 1990s from my translational radiation biology re-
Health Phys. 118(4):349–353; 2020 search (before it was called that) at Harvard Medical School
Key words: National Council on Radiation Protection and Measure- having discussions with my colleague Kathy Held at the
ments; nuclear terrorism; radiation emergency; radiation oncology Massachusetts General Hospital. In accordance with the
theme of this 90th anniversary of NCRP, which is defined
as “Providing Best Answers to Your Most Pressing Ques-
tions about Radiation,” I discuss from my vantage point in
INTRODUCTION the NCI Radiation Research Program, “What are the new
frontiers for the NCRP with its breadth of talent and exper-
ON BOTH a personal and professional level, it is an honor for tise in the rapidly evolving era of precision medicine?”
my research and that of my clinical and policy-minded col- Rather than an encyclopedic review, this concept paper
leagues to be recognized. Surveying the prior Warren Sin- with three closely related themes uses selected data and in-
clair Keynotes (NCRP 2019) since their inception in 2004, formation from both my laboratory and policy work along
this lecture fits squarely within over half the talks, including with that of my colleagues to describe unique opportunities
radiological terrorism (Poston 2005; Covello 2011; Herrmann surrounding this question. I recognize that many others con-
tribute to these three topics.
1
Radiation Research Program, Division of Cancer Treatment and Di-
agnosis and Radiation Oncology Branch, Center for Cancer Research, Na-
tional Cancer Institute, Bethesda, MD; 2Office of the Assistant Secretary
of Preparedness and Response, Department of Health and Human Ser- DISCUSSION
vices, Washington, DC.
The authors declare no conflicts of interest. When considering the frontiers of medical radiation
For correspondence contact the author at Radiation Research Program,
Division of Cancer Treatment and Diagnosis and Radiation Oncology science and the potential for NCRP, a good starting point
Branch, Center for Cancer Research, National Cancer Institute, Bethesda, is the breadth of the role of radiation science in federal agen-
MD, or email at ccoleman@mail.nih.gov. cies and through them, via collaborations and funding, the
(Manuscript accepted 5 November 2019)
0017-9078/20/0 academic and private sectors. Radiation and its interactions
Copyright © 2020 Health Physics Society with people are essential scientific topics for the National
DOI: 10.1097/HP.0000000000001240 Institutes of Health (NIH), in particular NCI, but also other
www.health-physics.com 349

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350 Health Physics April 2020, Volume 118, Number 4

institutes where radiation may be used for immune modula- Cornell Medical Center; and Chip Petricoin and Lance
tion, such as the National Institute of Allergy and Infectious Liotta, George Mason University), we have demonstrated:
Diseases (NIAID). Research is conducted into the normal
tissue effects from radiation exposure and potential means 1. Multi-fraction (MF110) (1 Gy twice daily  10 over 5
to mitigate such effects in the Radiation and Nuclear Coun- d) compared to SD (10 Gy 1) for prostate cancer cells
termeasures Program of NIAID (2013), the National Aeronau- in vitro (John-Aryankalayil et al. 2010; Makinde et al.
tics and Space Administration (NASA 2019) Human Research 2013) and in three-dimensional cultures (Eke et al.
Program, and the US Department of Defense Armed Forces 2018a) produces many more changes in gene expres-
Radiobiology Research Institute (USU 2018). Other agen- sion at the end of radiation, although there are changes
cies have interest in environmental or industrial radiation after both MF and SD. Interestingly, recent data looking
exposure [such as the US Environmental Protection Agency at long-term survivors after 2 mo shows this pattern re-
(US EPA 2019)] and radiation as an energy source (the De- versed with SD > MF (Eke et al. 2018b). We are currently
partment of Energy and the Nuclear Regulatory Commission). investigating what these adaptations are, how the cells
The critical need for the National Institute of Standards and have adapted, and how to target the adaptation:
Technology may be more essential than appreciated in ra- 2. In the 5 d (1 Gy twice a day) studies, there is an inflec-
diobiology (Desrosiers et al. 2013). tion point of gene expression after six to seven fractions,
when cells are given treatment with 1 Gy either two or
Theme #1: A new concept of defining radiation dose in three times per day. The gene ontology class with the
biological as well as physical terms most changes is immune response (John-Aryankalayil
Around 2004, our translational laboratory-clinical et al. 2010), but there are other changes seen with prote-
research team was developing the use of nonsteroidal anti- omics and metabolomics that are potentially targetable
inflammatory agents as clinical radiation sensitizers for pros- (Makinde et al. 2013). In the initial SD and MF studies
tate cancer based on preclinical data from work done at the by Tsai et al. (2007) in Jim Mitchell’s laboratory, changes
Harvard Joint Center for Radiation Therapy (Palayoor et al. are observed in vivo as well as in vitro.
1998). At the time, we sought biomarkers of drug effect prior 3. In proof-of-principle studies, molecular targets induced
to a clinical trial as is now required. We used gene expression both short-term (immediately after) (Eke et al. 2018a)
arrays following three conditions: (1) the nonsteroidal anti- and long-term (months later) (Eke et al. 2018b) can be
inflammatory agent drug concentrations (both COX2 and targeted with drug treatment post-exposure.
nonspecific COX inhibitors) used in most laboratory exper- 4. The initial tumor gene expression profile does not pre-
iments to determine mechanism of action, (2) the concen- dict the adaptive response. This has implications for
tration actually achievable in the clinic, and (3) molecular how to use molecular profiling for determining a course
techniques (RNAi) to knock down expression of the COX2 of cancer treatment, suggesting the need for repeat inter-
protein that is the primary target of the COX2 inhibitors. We rogation beyond the initial profile used for diagnosis. It
found that the clinically achievable drug concentration had may be that repeated interrogation and treatment ad-
very limited efficacy (John-Aryankalayil et al. 2009), and aptation will be necessary. These could involve both
thus we did not conduct a clinical trial. This turned out to imaging and investigating tumor samples or circulating
be a correct assessment as the drug was demonstrated to biomarkers, as are in progress.
not be effective in a number of clinical trials. This observa- 5. From work of our NCI (Mansoor Ahmed and Jim Hodge)
tion led us to consider the question of what happens to cells (Aryankalayil et al. 2014) and Cornell (Vanpouille-Box
and tumors that survive multiple fractions of clinically rele- et al. 2017) collaborators (above), the immune response
vant radiation therapy with the hypothesis that “adaptation to immune checkpoint inhibitors can be enhanced, and
to radiation therapy may induce changes across tumor types the fractionation pattern matters in the production of
that can be targets for molecular-targeted therapy.” This is the abscopal response (in which treatment of the pri-
different than using radiation plus drugs together, which mary tumor causes a response in metastases).
is often called chemo-radiotherapy; rather, this work aims 6. Changes with MF and SD are seen in short-term cultures of
to administer a fractionated or single dose (SD) of radia- endothelial cells (Palayoor et al. 2014) so that normal tissues
tion to make drugs work after the radiation is finished. also respond differently to radiation fractionation and dose.
Certainly, this would be compatible with the current uses 7. Using MF 0.5Gy  10 that produces very little cell kill-
of chemo-radiotherapy. ing can induce changes (Simone et al. 2013). This im-
To briefly highlight over 15 y of research in our labora- pacts normal tissues even distant to the tumor.
tory and those of our collaborators (James Mitchell, Radiation
Biology Branch, NCI; Silvia Formenti, Sandra Demaria, A 2017 NCI workshop “Defining the Shades of Gy:
Claire Vanpouille-Box, New York University and now Weill Utilizing the Biological Consequences of Radiotherapy in
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Warren K. Sinclair Keynote c C. N. COLEMAN 351

the Development of New Treatment Approaches” has ad- expertise being involved directly with the major decision
ditional information on the concept of using both the makers during a radiation/nuclear incident due to the com-
physical dose and biological perturbations for cancer treat- plex physics, biology, spectrum of injury, and medical care
ment (Ahmed et al. 2018). and for the public’s concern about radiation exposure. The im-
The various “omics” in biology, including coding and portance of this was learned from first-hand experience as part
non-coding RNA, metabolomics, and proteomics, are now of a team of subject matter experts in the US Embassy in
used to understand cancer biology, patient prognosis, and treat- Tokyo during the nuclear power plant crisis in Fukushima
ment effect. In a concept proposed by our laboratory in 2000 in 2011 (Simon et al. 2012; Coleman et al. 2013; Koerner et al.
dubbed “focused biology” (Coleman 2003), the aim is to 2014). Building on a concept proposed by Irwin (Koerner et al.
consider radiation “as a drug” assessing the pharmacokinet- 2014) for the creation of the Radiological Operations Sup-
ics and pharmacodynamics from radiation as is done with port Specialist (Irwin 2018), a major effort has been under-
systemic therapies. This novel approach uses the ability to taken by experts from government, academia, and the
focus the radiation delivery, thus adding up to “accurate, community to propose a new category of medical expertise,
precision radiation medicine.” the CBRNE Medical Officer Science Support Expert
(Coleman et al. 2019). The new opportunities for radiation
Theme #2: Radiological and nuclear incidents and the scientists in the first two themes relate to basic research,
need for medical and radiobiological expertise clinical care and emergency preparedness and response, in-
A number of laboratories, including ours, are investigat- cluding discovery and validation of biomarkers that can be
ing normal tissue response using molecular profiling sup- relevant for normal tissue damage for cancer care and for
ported by both NIAID and Biomedical Advanced Research population or industrial radiation exposure. Theme #3 ex-
and Development Authority (DHHS 2019) with the goal of pands the opportunities for radiation science even further.
establishing biomarkers for normal tissue injury from radiolog-
ical or nuclear incidents (Aryankalayil et al. 2018a and b). Such Theme #3. Accurate, precision radiation medicine
biomarkers may also be useful for clinical radiation therapy. A few years ago, colleagues from the NCI Radiation Re-
Pertinent to this lecture is the importance of subject matter search Program and CERN/Geneva were considering future

Fig. 1. The Radiation Rotary. There are a number of crossroads facing the field of radiation sciences, best addressed as part of a rotary. Four sets of
issues are illustrated, with both sides of a particular issue in circles of the same shade: (1) cancer care; (2) global collaboration; (3) nuclear policy;
and (4) mitigating radiation injury, as discussed in the text. Talent and ideas entering the rotary face challenges and choices that will lead to unique
collaborations, new knowledge, and products that, in turn, will impact greater society in general. The scope of talent and opportunities is large. Even
in the more limited context of cancer treatment, a wide range of expertise is needed to carry out the work intended in the radiation rotary, including
specialized chemistry, physics, biology, and medical skills. Abbreviations: IGRT—image guided radiation therapy; LINAC—linear accelerator
(Coleman et al. 2018; reprinted with permission).
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352 Health Physics April 2020, Volume 118, Number 4

possibilities for radiation research and described a number of molecular signature of pro-immunogenic radiotherapy targets
“crossroads.” Recognizing that seemingly disparate radiation in human prostate cancer cells. Radiat Res 182:139–148; 2014.
Aryankalayil MJ, Chopra S, Levin J, Eke I, Makinde A, Das S,
science careers intersect much more than may be recognized, Shankavaram U, Vanpouille-Box C, Demaria S, Coleman CN.
we proposed the idea of the Radiation Rotary (Coleman Radiation-induced long noncoding RNAs in a mouse model af-
et al. 2018) (Fig. 1) in which four sets of crossroads come ter whole-body irradiation. Radiat Res 189:251–263; 2018a.
together. The figure (reprinted with permission) is largely Aryankalayil MJ, Chopra S, Makinde A, Eke I, Levin J, Shankavaram U,
MacMillan L, Vanpouille-Box C, Demaria S, Coleman CN. Micro-
self-explanatory, where opposite sides are contrasts of the array analysis of miRNA expression profiles following whole body
same theme (shaded circles) but all of the themes interact. irradiation in a mouse model. Biomarkers 23:689–703; 2018b.
Opportunities that can impact society are noted. Bernhard E, Blumenthal D, Boice J, Coleman N, Maidment B,
Among the challenges for NCRP is addressing the issue Miller C, Noska M, Schauer D, Toohey R, Whitcomb R. National
crisis “Where are the Radiation Professionals?” [online]. 2013.
proposed by John Boice in the NCRP report of “WARP— Available at https://ncrponline.org/wp-content/themes/ncrp/
Where are the Radiation Professionals?” (Boice 2014). Dis- PDFs/WARP_Workshop_Summary.pdf. Accessed 20 July 2019.
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to the following proposal: the training of molecular radiation Phys News XLII:22; 2014.
Brink JA. Fourth Annual Warren K. Sinclair Keynote Address.
epidemiologists building from radiation oncologists who have The use and misuse of radiation in medicine. Health Phys 95:
expertise in clinical medicine who will acquire further training 465–501; 2008.
in molecular cancer biology and epidemiology to become Bushberg JT. Eleventh Annual Warren K. Sinclair Keynote Address—
MD- or PhD-level molecular radiation epidemiologists. A science, radiation protection and NCRP: building on the past,
looking to the future. Health Phys 108:115–123; 2015.
proposal for NCRP to consider such a path, working with Coleman CN. Linking radiation oncology and imaging through
a few medical schools that also have schools of public health, molecular biology (or now that therapy and diagnosis have sep-
was submitted at the 2019 NCRP business meeting. Should a arated, it's time to get together again!). Radiol 228:29–35; 2003.
few pilot programs be successful, this may produce a new ca- Coleman CN, Blumenthal DJ, Casto CA, Alfant M, Simon SL,
Remick AL, Gepford HJ, Bowman T, Telfer JL, Blumenthal
reer path for this critical expertise for academia, govern- PM, Noska MA. Recovery and resilience after a nuclear power
ment agencies, and the private sector and expand the role plant disaster: a medical decision model for managing an effec-
of physician-scientists in epidemiology of radiation expo- tive, timely, and balanced response. Disaster Med Public Health
sures and possibly other environmental factors as well. Prep 7:136–145; 2013.
Coleman CN, Prasanna PGS, Bernhard EJ, Buchsbaum JC, Ahmed
MM, Capala J, Obcemea C, Deye JA, Pistenmma DA, Vikram
CONCLUSION B, Bernier J, Dosanjh M. Accurate, precision radiation medi-
cine: a meta-strategy for impacting cancer care, global health,
There are remarkable opportunities for the application and nuclear policy and mitigating radiation injury from necessary
of emerging cancer and radiation biology to further enhance medical use, space exploration, and potential terrorism. Int J
the contributions by NCRP and other radiation-related socie- Radiat Oncol Biol Phys 101:250–253; 2018.
Coleman CN, Bader JL, Koerner JF, Hrdina C, Cliffer KD, Hick JL,
ties and fields. The role of radiation in a broad range of soci- James JJ, Mansoura MK, Livinski AA, Nystrom SV, DiCarlo-
etal needs, including medical care, energy policy, terrorism, Cohen A, Marinissen MJ, Wathen L, Appler JM, Buddemeier
space exploration, environmental exposures and global B, Casagrande R, Estes D, Byrne P, Kennedy EM, Jakubowski
health, provides exciting opportunities for radiation exper- AA, Case C, Weinstock DM, Dainiak N, Hanfling D, Garrett
AL, Grant NN, Dodgen D, Redlener I, MacKAY TF, Treber M,
tise (Bernhard et al. 2013) Homer MJ, Taylor TP, Miller A, Korch G, Hatchett R. Chemical,
biological, radiological, nuclear, and explosive (CBRNE) sci-
Acknowledgments—to multiple colleagues who are co-authors of the references
and many others who participate in the programs and projects described in this
ence and the CBRNE medical operations science support expert
manuscript. (CMOSSE). Disaster Med Public Health Prep 1–16; 2019.
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of Health, U.S. Department of Health and Human Services, or U.S. Government. gencies, tools, and techniques. Health Phys 101:511–530; 2011.
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Warren K. Sinclair Keynote c C. N. COLEMAN 353

Herrmann J. Fourteenth Annual Warren K. Sinclair Keynote Address: immune response pathway transcripts and miRNAs in normal
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