comments and controversies

Low-Grade Prostate Cancer: Time to Stop

Calling It Cancer
Scott E. Eggener, MD1; Alejandro Berlin, MD2; Andrew J. Vickers, PhD3; Gladell P. Paner, MD4; Howard Wolinsky5; and
Matthew R. Cooperberg, MD6

Introduction PCa.3 GS6 is largely a natural, age-related histologic

Prostate-specific antigen (PSA) screening for prostate observation defined artefactually as a disease, not
cancer (PCa) remains highly controversial, largely known to cause symptoms or metastases,6 but para-
because it is unclear whether the primary benefits of doxically leads to invasive monitoring or treatment.
reducing rates of metastases and cancer mortality are These concerns were a primary factor contributing to
worth the risks of overdiagnosis, overtreatment, and the US Preventive Services Task Force categorically
potential treatment-related morbidity. A major con- discouraging PCa screening in 2012, specifically
tributing factor to overdiagnosis and overtreatment is noting the common diagnosis and treatment of “mi-
the designation of a particular pattern of low-grade croscopic, well-differentiated lesions…unlikely to be
cellular changes in the prostate as cancer, which, in clinically important.”7
our view, should not be called cancer. A simple ter- Low-Grade Prostate Cancer Behaves Clinically Like
minology change for these lesions and removal of the Precancer Rather Than Cancer
cancer label would dramatically reduce overdiagnosis
and overtreatment and markedly change the cost- A common definition of cancer is a “malignant tumor
benefit calculus of PSA screening. Although pro- (which) can invade and destroy adjacent structures
posed previously,1,2 it never became a widespread and spread to distant sites,”8 a view generally shared
discussion with material impact. We feel that revisiting by the nonmedical public.9 Although GS6 meets the
this proposal is timely, compelling, relevant, and of pathologic criteria of a cancer (invasion of the stroma),
utmost importance. without the simultaneous presence of higher-grade
disease (GS $ 7; ie, Grade Group $ 2), it is effec-
The histologic grading system for PCa encompasses tively incapable of invading adjacent local structures10
remarkable diversity—from nearly universal indolence or metastasizing.11 When a prostate is surgically re-
(Gleason score [GS] 6) to almost certain eventual le- moved and contains only GS6, there is essentially a
thality (GS10)—and drives nearly all management 100% chance of remaining metastasis-free12 although
decisions in localized PCa. We review the inert clinical the cancer has typically been present for years and
behavior of GS6 PCa, ongoing concerns regarding often decades. When a cancer-related death rate
widespread overdiagnosis and overtreatment, and the approaches 0%, even in the absence of treatment,
rationale for a change in nomenclature. consideration should be given to modifying the
ASSOCIATED
CONTENT screening, diagnostic, management, and terminology
GS6 Histology is Highly Prevalent paradigms.
See accompanying
article on page 3106 After rapid and pervasive adoption of PSA-based early
detection efforts in the United States, the age-adjusted Contemporary Detection and Management of GS6
Author affiliations
and support PCa-specific mortality decreased by 50% and is Reflects a Precancer Rather Than Cancer
information (if certainly reason for celebration.3 However, the unin- Modifications to early detection paradigms have oc-
applicable) appear
tended consequences of this pyrrhic victory adversely curred and are ongoing. Indiscriminate screening is
at the end of this
article.
affected millions of men diagnosed with and treated for less common, but remains highly prevalent. Novel
Accepted on March
cancers never destined to alter their quality or quantity blood and urine biomarkers and magnetic resonance
16, 2022 and of life.4 PCa incidence doubled,5 with low-grade imaging (MRI) have been integrated into diagnostic
published at cancers such as GS6 (ie, Grade Group 1) account- pathways as secondary tests to identify higher-grade
ascopubs.org/journal/ ing for up to 70% of new diagnoses.2,3 The root of the cancers while attempting to minimize the number of
jco on April 18, 2022:
overdiagnosis epidemic stems from . 30% of men men diagnosed with GS6.13-15 Clinical management of
DOI https://doi.org/10.
1200/JCO.22.00123
over age 50 (more than 60% by age 80) years harbor GS6 has dramatically changed following institutional
© 2022 by American
histologic PCa, as microscopic PCa ultimately de- series, clinical trials, and population-based data
Society of Clinical velops in nearly all prostates if a man lives long showing superb long-term outcomes with various
Oncology enough.4,5 Yet, only 3% of all men eventually die of forms of conservative management (ie, active

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Low-Grade Prostate Cancer: Time to Stop Calling It Cancer

surveillance),16-19 including similar PCa mortality rates and has been discussed for other cancers such as breast
compared with matched populations of men without PCa.20 (low-grade ductal carcinoma in situ)33 and melanoma
Consequently, active surveillance is now a global standard (Fig 1).34 A commonality among many of these cancers is
of care21 and used frequently, in up to 80% of men with low- the high prevalence of indolent disease in the healthy
risk PCa in Sweden,22 Canada,23 and parts of the population. Although not a new conversation in PCa, the
United States.24 However, in many countries and most compelling supportive data amplify the urgency of the
regions of the United States, underutilization of active message.
surveillance remains common25 as many physicians—both
Advantages of Renaming GS6
primary care doctors and PCa specialists—continue to
routinely recommend treatment.26 Reclassification of GS6 would immediately lead to
markedly fewer diagnoses of PCa; fewer men receiving
GS6 Should be Renamed radiation, surgery, and other treatments; fewer men ex-
Concordant with these commendable efforts in modifying periencing treatment-related side effects; lower patient
screening, diagnosis, and management, strong consider- and family anxiety; and substantial reductions in financial
ation should also be given to eliminating the word cancer burden to individuals and the health care system.35 No
from GS6. PCa experts have previously debated reclassi- matter how much time a physician may spend down-
fication of GS6 and removal of the cancer label.1,2,27 playing the significance of a GS6 diagnosis or emphasizing
Similarly, a Centers for Disease Control and Prevention the phrase low-risk, the words “you have cancer” have a
(CDC) State-of-the-Science Consensus meeting in 2012 on potent psychological effect on most men and their
the role of active surveillance in the management of men families.
with low-risk PCa recommended the development of new A PCa diagnosis has been associated with an increased risk
terminology to replace the word cancer and supported the of depression and suicide,36 even when low-grade, despite
classification of low-risk lesions as indolent lesions of ep- negligible risk of cancer-related harm. Even when a patient
ithelial origin.28 However, the massive issue of over- chooses surveillance, family or friends of patients may often
diagnosis and overtreatment persists. Revisiting this find the decision to live with untreated cancer bizarre.
discussion should be a high priority within the PCa Frustratingly, when purchasing life insurance policies, the
community. diagnosis can lead to disqualification or considerably
Reclassifying cancer has precedent—in prostate (GS 2 higher rates. Since many guidelines and policymakers
through 5),29 bladder,30 cervical,31 and thyroid cancers32— advocate shared decision making,37 it is critical to consider

The Problem: An Epidemic of Over Diagnosis Ongoing and Suggested Strategies to Mitigate
Unnecessary Diagnosis and Treatment
Over 50% of men over the
Worldwide, hundreds of
age of 50 years have histologic
thousands of men diagnosed > 50% prostate cancer Smarter Screening
annually with Gleason score
6 disease. Selective screening based on risk, life expectancy, and patient preference
Increased use of serum, urine, and genetic biomarkers
Up to 50% of men with
$ Gleason score 6 are treated Tailored Diagnosis and Management
50% with radiation or surgery
Increase the clinical threshold to biopsy
MRI to minimize diagnosis of indolent disease and optimize biopsy quality
Appropriate utilization of surveillance strategies for early-stage disease
In the PSA era, millions of 15-year rates of metastases or
men are unnecessarily diagnosed cancer-specific death are less
and treated, costing billions < 1% than 1% in men with only GS 6 Nomenclature Change
of dollars.
Multidisciplinary discussion to modify the definition of prostate cancer

Removing the "Cancer" Label From Indolent Lesions: Precedents and Ongoing Debates ENACTED DISCUSSED

Bladder (urothelial): PUNLMP Thyroid: NIFTP

Prostate: GS 2-5 Cervix: SIL Breast DCIS Melanoma
Papillary Urothelial Neoplasm of Low Non-Invasive Follicular Thyroid Neoplasm
Gleason Score Squamous Intraepithelial Lesion Thyroid Prostate: Gleason Score 6
Malignant Potential With Papillary-like Nuclear Features

1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020 2021

FIG 1. Low-grade prostate cancer: prevalance of overdiagnosis, mitigation strategies, and historical parallels. DCIS, ductal carcinoma in situ; PSA,
prostate-specific antigen.

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Eggener et al

a more patient-centric disease labeling to promote clarity (to noncancers or GS6) and when active surveillance for low-
and understanding, provide value, and limit undue harm. grade PCa was introduced in the mid-1990s. Countless other
clearly positive transformations in PCa and throughout the
Common Counterarguments to Renaming GS6
oncology and medical sciences were initially and continu-
The most common counterargument for preserving the ously met with doubt and even scorn, yet proven unequiv-
current nomenclature is that up to 30% of men with GS6 ocally correct by history.
on biopsy who undergo surgery are found to harbor
higher-grade cancers.38 Nonetheless, the presence of Intent of Contemporary Prostate Cancer Screening
higher-grade cancers unsampled on biopsy does not de- Most experts agree that the modern objective of PCa
monstrably alter long-term oncologic outcomes.39 The screening in an otherwise healthy man who chooses to
flawed rationale of routinely treating men with GS6 on biopsy undergo screening is to identify GS $ 7 cancers while
on the basis of the possibility of unsampled higher-grade curtailing the diagnosis of GS6. Accordingly, the National
cancers would be similar to treating a man with a negative Comprehensive Cancer Network (NCCN) PCa Early De-
biopsy on the basis of similar concerns, a strategy that would tection Guidelines state that screening should “improve the
universally be considered improper. In the contemporary identification of significant cancer while avoiding the de-
era—with MRI, image-directed biopsies, more extensive tection of indolent disease”.42 What is a better way to
biopsy sampling templates, restaging biopsies during sur- avoid the detection of GS6 than to retire its cancer label
veillance, and integration of genomic biomarkers—rates of entirely?
identifying higher-grade cancers on subsequent biopsy
Radical treatment for a relabeled GS6 may one day be
in men whose initial biopsy showed GS6 are strikingly
considered inappropriate and unjustifiable in most cases.
similar (20%-30%) to rates of identifying higher-grade
We envision a landscape in which treatment for localized
cancers among men who undergo surgery for GS6 on
PCa would nearly always require the presence of GS $ 7 or
biopsy.40
other objective evidence of adverse biology. Similar to
Advocates of preserving the status quo of categorizing GS6 current management of noncancerous prostate lesions
as cancer suggest that active surveillance with PSA, digital such as high-grade prostatic intraepithelial neoplasia and
rectal examination, and intermittent biopsies (with or atypical small acinar proliferation, a variety of individualized
without MRI) are essential to diagnose previously un- risk-stratified screening options would be available for
identified or newly formed higher-grade cancers in a timely erstwhile GS6, including ongoing screening, biomarkers,
fashion. Relabeling GS6 would not lead to recategorizing imaging, and rebiopsy.
these biopsies as normal, and therefore, a diagnosis would
still indicate a similar approach of serial PSA (with or Renaming GS6 is Important for Public Health
without other biomarkers), digital rectal examination, and A sensible path forward requires input from many stake-
MRI (with or without biopsies). By analogy, colon polyps holders, including pathologists, urologists, radiation on-
warrant a varying intensity of surveillance and endoscopy cologists, patients, and partners. The exact relabeling is not
on the basis of the risk profile, but without the label of pertinent except for it not including cancer, as most people
cancer, they preclude any question of routine colectomy or understandably associate the word with an aggressive and
chemoradiation therapy. possibly lethal malady. Regardless of what tempering terms
might be used, if the disease label includes cancer, it af-
Another criticism of the proposed nomenclature change is
fects mental health, modulates decisions and behavior, and
that approximately 15% of GS6 cancers have molecular
increases tolerance for treatment-derived toxicities.43 In
similarities to higher-grade cancers.41 Although true, this is
breast cancer, as in PCa, nomenclature directly affects the
challenging to reconcile with, to our knowledge, the ab-
likelihood of patients electing aggressive treatment.33,44
sence of any patient with pure GS6 ever experiencing a
Every PCa clinician observes this phenomenon on a reg-
metastasis or death from the cancer. GS6 labeled some-
ular basis.
thing other than cancer would still require surveillance, and
since the window of opportunity for curing localized PCa is The conversation is necessary and should be multidis-
typically measured in years or decades, evidence of his- ciplinary, but the ultimate nomenclature decision will
tologic progression to a higher-grade cancer would far depend on genitourinary pathologists, ideally with input
precede the potential time of future metastasis in the from other specialists and patient advocates. We feel that
majority of cases. platforms within individual specialty meetings, multidis-
There may be legitimate concerns about patient com- ciplinary conferences, and even symposiums singularly
pliance with ongoing surveillance for a precancerous focused on GS6 are key to addressing this important
lesion, potential delays in diagnosing higher-grade can- public health issue.
cers, debate over the intensity and type of follow-up, and Even if GS6 is biologically inert, its labeling is not, as it has
impact on longer-term cancer outcomes. Similar con- an important influence and tangible consequences on how
cerns were raised when GS 2-5 tumors were reclassified patients, providers, and the general public react and

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Low-Grade Prostate Cancer: Time to Stop Calling It Cancer

respond. We believe that a name change should be thor- implementation efforts. Nevertheless, we feel that rescinding
oughly discussed, vetted, and ultimately adopted. If ultimately the cancer label from GS6 would dramatically improve in-
deemed appropriate, there will be predictable and unforeseen dividual and public health. The data are compelling, the moral
obstacles, requisite educational campaigns, and large-scale imperative is sound, and the time is overdue.

AFFILIATIONS AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF

1
Section of Urology, University of Chicago, Chicago, IL INTEREST
2
Department of Radiation Oncology, University of Toronto, Toronto, Disclosures provided by the authors are available with this article at DOI
Canada https://doi.org/10.1200/JCO.22.00123.
3
Department of Epidemiology and Biostatistics, Memorial Sloan-
Kettering Cancer Center, New York, NY
4
Department of Pathology, University of Chicago, Chicago, IL
AUTHOR CONTRIBUTIONS
5
Patient-Advocate, Answer Cancer Foundation, Chicago, IL Conception and design: All authors
6
Department of Urology, University of California—San Francisco, San Data analysis and interpretation: All authors
Francisco, CA Manuscript writing: All authors
Final approval of manuscript: All authors
Accountable for all aspects of the work: All authors
CORRESPONDING AUTHOR
Scott E. Eggener, MD, University of Chicago, 5841 South Maryland, Mail
Code 6038, Chicago, IL 60637; e-mail: [email protected].
ACKNOWLEDGMENT
We acknowledge Adam Badzynski, medical illustrator, for the figure.

EQUAL CONTRIBUTION
S.E.E. and A.B. are coprimary authors.

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n n n

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Low-Grade Prostate Cancer: Time to Stop Calling It Cancer

AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

Low-Grade Prostate Cancer: Time to Stop Calling It Cancer
The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted.
Relationships are self-held unless noted. I 5 Immediate Family Member, Inst 5 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/jco/authors/author-center.
Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).

Scott E. Eggener commercialized by OPKO as the 4Kscore. I receive royalties from sales of the
Consulting or Advisory Role: Sophiris Bio, Francis Medical, Insightec, Profound 4Kscore
Medical, Candel Therapeutics Travel, Accommodations, Expenses: OPKO Health
Speakers’ Bureau: Janssen
Gladell P. Paner
Travel, Accommodations, Expenses: Janssen Biotech, Insightec
Honoraria: Amirsys
Uncompensated Relationships: Steba Biotech
Matthew R. Cooperberg
Alejandro Berlin
Consulting or Advisory Role: Astellas Pharma, Dendreon, AstraZeneca, Bayer,
Consulting or Advisory Role: AbbVie, Ferring, Astellas Pharma
Merck, Exact Sciences, Veracyte, Verana Health, ConcertAI, Pfizer
Research Funding: AbbVie
No other potential conflicts of interest were reported.
Andrew J. Vickers
Stock and Other Ownership Interests: OPKO Health
Consulting or Advisory Role: OPKO Diagnostics, Insightec, Steba Biotech
Patents, Royalties, Other Intellectual Property: I am named on a patent for a
statistical method to detect prostate cancer. This method has been

Journal of Clinical Oncology

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