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AACE/ACE Disease State Commentary
AMERICAN ASSOCIATION OF CLINICAL ENDOCRINOLOGISTS
AND AMERICAN COLLEGE OF ENDOCRINOLOGY DISEASE STATE
COMMENTARY: MANAGING THYROID TUMORS DIAGNOSED AS
NONINVASIVE FOLLICULAR THYROID NEOPLASM
WITH PAPILLARY-LIKE NUCLEAR FEATURES
Zubair W. Baloch, MD, PhD1; R. Mack Harrell, MD, FACP, FACE, ECNU2;
Elise M. Brett, MD, FACE, CNSC, ECNU3; Gregory Randolph, MD, FACS, FACE4;
Jeffrey R. Garber, MD, FACP, FACE5;
On behalf of AACE Endocrine Surgery Scientific Committee and Thyroid Scientific Committee
ABSTRACT
EXECUTIVE SUMMARY
This commentary summarizes the history and reclassification of noninvasive follicular thyroid neoplasm with
papillary-like nuclei (NIFTP). It reviews the salient histopathologic features that are based on immunohistochemical
and molecular profiles and serve as inclusion and exclusion
criteria. The authors also provide their own point of view
regarding the practical issues and possible concerns that
may be raised by both clinicians and patients based on the
diagnosis of NIFTP. (Endocr Pract. 2017;23:1153-1158)
Historically, the definition of papillary thyroid carcinoma (PTC) versus follicular thyroid carcinoma was predicated on the predominant tumor growth pattern. Thus if
the tumor was mostly follicular in pattern on low-power
microscopic examination, it was classified as “follicular carcinoma” (1,2). Once the importance of nuclear
morphology was appreciated in the diagnosis of PTC (3),
experts agreed that thyroid epithelial cell tumors should be
identified as papillary by nuclear features, whether or not
papillary or follicular architecture was present (4).
The “follicular variant of papillary thyroid carcinoma”
(FVPTC) was described in the mid-1970s as a tumor with
a predominantly follicular growth pattern and the nuclear cytomorphology of PTC (4). Following this, 2 major
subtypes of FVPTC were described: infiltrative and encapsulated (5,6). Accumulated data suggest that infiltrative
FVPTC, which grows in the manner of follicular carcinoma with invasion into either its thick capsule or vessels
within the capsule, is more likely to behave aggressively.
In contrast, noninvasive encapsulated FVPTC (EFVPTC)
has been observed to behave in a benign fashion like follicular adenoma (7-10). This variable morphologic and clinical course has led to much controversy in the diagnosis
and management of noninvasive EFVPTC. Confusion has
been amplified by the lack of interobserver agreement on
the minimal diagnostic criteria for EFVPTC among endocrine pathology experts, causing angst among pathologists
and clinicians alike (11,12). Recent clinical follow-up
and case-control studies have confirmed that noninvasive
EFVPTC behaves in a benign fashion and may be overtreated (10,13). Moreover, recent molecular analyses of
EFVPTC tumors have suggested that these tumors may
have a unique set of genetic mutations and fusions (14-17).
Abbreviations:
AACE = American Association of Clinical
Endocrinologists; EFVPTC = encapsulated FVPTC;
FNA = fine-needle aspiration; FVPTC = follicular
variant of papillary thyroid carcinoma; NIFTP = noninvasive follicular thyroid neoplasm with papillary-like
nuclear features; PTC = papillary thyroid carcinoma
Submitted for publication April 27, 2017
Accepted for publication June 8, 2017
From the 1Hospital of the University of Pennsylvania, Perelman School
of Medicine, Philadelphia, Pennsylvania; 2Memorial Health Systems,
Inc, Memorial Center for Integrative Endocrine Surgery, Hollywood,
Florida; 3Division of Endocrinology, Diabetes and Bone Disease, Icahn
School of Medicine at Mount Sinai, New York, New York; 4Mass Eye and
Ear Infirmary/Mass General Hospital, Harvard Medical School, Boston,
Massachusetts; 5Endocrine Division, Harvard Vanguard Medical Associates,
Boston, Massachusetts, Division of Endocrinology, Beth Israel Deaconess
Medical Center, Boston, Massachusetts.
Address correspondence to Dr. Zubair W. Baloch; Hospital of the University
of Pennsylvania, Perelman School of Medicine; 6 Founders, Rm 6.043, 3400
Spruce Street, Philadelphia, PA 19104.
E-mail: baloch@mail.med.upenn.edu
Published as a Rapid Electronic Article in Press at http://www.endocrine
practice.org. DOI:10.4158/EP171940.DSCR
To purchase reprints of this article, please visit: www.aace.com/reprints.
Copyright © 2017 AACE.
Copyright © 2017 AACE
ENDOCRINE PRACTICE Vol 23 No. 9 September 2017 1153
1154 Managing Thyroid Tumors Diagnosed as NIFTP, Endocr Pract. 2017;23(No. 9)
In response to the confusion, a multidisciplinary panel,
the Endocrine Pathology Society (EPS) Working Group
including thyroid pathologists, endocrinologists, and an
endocrine surgeon, was established to address the important controversies surrounding the diagnosis of encapsulated and noninvasive FVPTC. The panel deliberations were
based on the clinical outcomes and tumor molecular analyses of a case cohort of noninvasive EFVPTC patients for
whom there was diagnostic consensus among the pathology experts in the group. All noninvasive EFVPTC patients,
followed for 10 to 26 years after diagnosis, were alive without evidence of disease. Importantly, none of these patients
received radioiodine ablation, and >50% were treated by
lobectomy only. In addition, molecular alterations typically
seen in classic PTC (BRAF V600E mutations or RET gene
fusions) were not seen in noninvasive EFVPTC cases. The
molecular profiles of these cases included RAS gene mutations (30% cases) and PPARG or THADA gene fusions
(44% cases). Based on the benign clinical outcomes and
characteristic molecular analysis data in these patients, the
Copyright © 2017 AACE
EPS Working Group recommended that truly noninvasive
EFVPTC tumors be redesignated as nonmalignant entity
termed “noninvasive follicular thyroid neoplasms with
papillary-like nuclear features” (NIFTP). This reclassification will have a significant effect on a large population of
patients worldwide, hopefully resulting in a diminution of
overaggressive treatment with a concomitant reduction in
clinical consequences and psychologic sequelae related to
the diagnosis of “cancer” (18). Although the case cohort
long-term outcome data supporting the nomenclature
change is strong, in the absence of prospective study confirmation, it is essential that endocrine physicians prospectively follow patients with NIFTP pathology to verify that
these patients’ postoperative courses are truly indolent.
NIFTP – DIAGNOSTIC CRITERIA
For optimal clinical management, it is important that
NIFTP is a surgical disease and this diagnosis cannot be
rendered on pre-operative fine-needle aspiration (FNA).
Table 1
Diagnostic Histopathologic Criteria for NIFTP
Diagnostic criteria
Comments
Inclusion criteria (Fig. 2 A-C)
1.
Well demarcated/encapsulated follicular patterned tumor
2.
Nuclear cytology of PTC
3.
Noninvasive characteristics
a.
No tumor capsule invasion or invasion into the
surrounding thyroid parenchyma
b.
No lymphovascular invasion
It is of utmost importance that a thorough sampling of tumor and its interface with
either tumor capsule or surrounding uninvolved thyroid parenchyma is carried out to
exclude invasive characteristics
Exclusion criteria
Invasion
•
Invasion beyond the periphery of tumor excludes the diagnosis of NIFTP
•
This includes invasion by the tumor cells into the tumor capsule,
extension into the surrounding thyroid parenchyma, and/or vascular
invasion into vessels within the tumor capsule or beyond
•
NIFTP predominantly shows a follicular growth pattern. However,
the presence of <1% papillary structuresa and ≤30% of solid growth
pattern (by area) is allowed (papillary structures are hallmark features of
conventional carcinoma)
•
Presence of any other growth patterns indicative of aggressive variants
of PTC such as tall cell, columnar cell, and hobnail variant exclude the
diagnosis of NIFT
•
Psammoma bodies represent “dead” papillary structures and can be seen
in tumor as well as within the lymphatics away from tumor
•
Any form of “true” tumor necrosis (excludes necrosis associated with
preoperative fine-needle aspiration) and or mitoses can be associated with
high-grade transformation and/or aggressive clinical behavior
•
Three or more mitotic figures in 10 consecutive high-power fields exclude
the diagnosis of NIFTP (this criterion requires future clinicopathologic
validation)
Tumor growth pattern
Lymphovascular invasion and/or lymph node metastases
Psammoma bodies
Tumor necrosis and or mitoses
Abbreviation: NIFTP = noninvasive follicular thyroid neoplasm with papillary-like nuclei.
aBased on a study by Cho et al (19), 3% lymph node metastases were noted in cases with a 1% cutoff value for papillary structures. These authors have
suggested not to render a diagnosis of NIFTP even in the presence of a single papillary structure.
Copyright © 2017 AACE
A
Managing Thyroid Tumors Diagnosed as NIFTP, Endocr Pract. 2017;23(No. 9) 1155
B
C
Fig. 1. NIFTP: Low-power view showing a thinly encapsulated noninvasive follicular patterned nodule (A-B) comprised of macro- and microfollicles lined
by cells showing papillary-like nuclei (C). NIFTP = noninvasive follicular thyroid neoplasm with papillary-like nuclei.
A
B
C
D
Fig. 2. A cartoon depiction of diagnostic criteria for encapsulated follicular lesions of the thyroid gland: follicular adenoma, follicular carcinoma, NIFTP,
and the follicular variant of papillary thyroid carcinoma (lightest blue, black asterisk = tumor capsule, medium blue = tumor, red asterisk = tumor cells
without nuclear features of PTC, darkest blue = invasive tumor). The follicular adenoma is encapsulated and shows no invasion (A), whereas the follicular
carcinoma shows tumor cells invading into or beyond the tumor capsule (red arrows) and/or showing vascular invasion into the capsular vessels (black
arrow, B). The NIFTP is an encapsulated tumor that shows PTC-like nuclei without invasive characteristics (C). The encapsulated follicular variant of PTC
shows nuclear features of PTC and invasion into or beyond the tumor capsule (red arrows) and/or vascular invasion (black arrows, D). NIFTP = noninvasive follicular thyroid neoplasm with papillary-like nuclei; PTC = papillary thyroid carcinoma.
The diagnosis of NIFTP be made with strict adherence to
the following inclusion and especially to, exclusion histomorphologic criteria (18) (Table 1, Fig. 1 and 2).
As mentioned above, the renaming of noninvasive
EFVPTC to NIFTP may prove to be beneficial to patients;
however, it may also raise the following questions for both
clinicians and patients:
Invasive Characteristics
The diagnosis of tumor capsule invasion can be a difficult task for the surgical pathologist, partly due to lack of
consensus among experts in defining the diagnostic criteria (8). Various criteria have been cited in the literature for
the diagnosis of invasion into the tumor capsule (8). Some
debate the importance of capsular invasion in the absence
of vascular invasion (20). Since it has been associated with
metastatic disease, any form of invasion by the tumor cells
into its capsule (usually traversing the entire thickness of
capsule) or into the surrounding normal thyroid parenchyma should exclude the diagnosis of NIFTP.
Multifocal Tumors and Staging
The diagnosis of NIFTP does not preclude the diagnosis of another distinct tumor(s) in the thyroid gland. Cancer
staging in such cases should not include NIFTP lesions.
Tumor Size
The NIFTP proposal study did not include tumors
measuring <1.0 cm; however, a recent study has shown that
these tiny tumors can be included in the new category (21).
A recent study by Xu et al demonstrated that NIFTP tumors
measuring ≥4.0 cm appear to have an extremely low risk
of recurrence, even when treated with conservative surgical treatment without radioiodine therapy (22). However,
1156 Managing Thyroid Tumors Diagnosed as NIFTP, Endocr Pract. 2017;23(No. 9)
the diagnosis of NIFTP in large-sized tumors should
only be entertained, when the entire tumor capsule has
been evaluated by histopathologic evaluation to exclude
invasive characteristics.
Impact of Preoperative FNA Diagnosis
The most important issue that has surfaced with the newly
created diagnosis of NIFTP is the inevitable increase in
the “false-positive” rates for cases diagnosed as suspicious or consistent with PTC by preoperative FNA cytology and molecular assessment (23-25). Recent studies
have shown that noninvasive EFVPTC have previously
comprised a significant proportion of malignant diagnoses associated with the indeterminate diagnostic categories of The Bethesda System for Reporting Thyroid
Cytology (TBSRTC) (26-29): atypia of undetermined
significance/follicular lesion of undetermined significance
(AUS/FLUS), follicular neoplasm/suspicious for follicular neoplasm (FN/SFN), and suspicious for malignancy
(14). However, one would predict no appreciable change
in the risk of malignancy for FNA cases diagnosed as
benign (Bethesda 2) and malignant (Bethesda 6) based on
the NIFTP nomenclature change. The initial studies have
shown an appreciable decrease in the rate of malignancy
for indeterminate categories of TBSRTC. The reported
ranges for changes in the rate of malignancy are AUS/
FLUS 19 to 45% to 15-30%, FN/SFN –22 to 45% to 10
to 37%, and SM 72 to 87% to 46 to 68% (24,25,29,30)
(Table 2) . Such alterations in the rate of malignancy for the
indeterminate diagnostic categories (Bethesda III-V) may
lead to changes in the thyroid nodule pre- and postsurgical management paradigms, especially for those classified
as SM, as recommended by the American Association of
Clinical Endocrinologists (AACE) and American Thyroid
Association for low-risk thyroid neoplasms (31-33). It is
hoped that with the emergence of this new nonmalignant
category, physicians may tend to recommend lobectomy
with greater assurance in patients with Bethesda III-IV
cytology, especially in those with RAS mutations and
PPARG or THADA gene fusions (18).
Recent retrospective studies have shown that NIFTP
comprises approximately 5% of thyroid FNA speci-
Copyright © 2017 AACE
mens diagnosed as malignant (25,28,30,36). Though
this percentage may not appear significant, even a small
decrease in risk of malignancy for the “malignant” FNA
category could raise concerns about potential medicolegal
implications in the pathology community. As a result, some
pathologists have suggested that the diagnosis of PTC in
FNA specimens be limited to cases that demonstrate diagnostic features of the classic or tall cell variants of PTC:
papillary architecture, psammomatous calcifications, and
well-formed pseudo-inclusions. Based on these potential
future concerns, some pathologists are now including an
explanatory note regarding the possibility that NIFTP
tumors are part of the differential diagnosis list for Bethesda
III-VI cytology results and that this new noncancerous
diagnostic category may change Bethesda III-V categorybased performance characteristics (25). It is also crucial to
understand and explain to patients that NIFTP is not a
“benign tumor” but a “low-risk neoplasm” that requires
surgical excision for diagnosis followed by comprehensive pathologic evaluation of the tumor contents and
its capsule. Moreover, it is reasonable to suggest that in
thyroid nodules demonstrating indeterminate or low-risk
ultrasound features, FNAs in the Bethesda III-V categories
and/or with NIFTP-suggestive molecular profiles (only
RAS-mutations and/or PPARG and THADA gene fusions,
without BRAF or TERT promoter mutations), conservative
management with hemithyroidectomy for diagnosis may
be the best surgical approach (18,23,25).
What to advise patients whose tumors have been reclassified as NIFTP? (37)
(1) “I was told that I had a follicular variant of papillary
carcinoma. Did I have cancer?” (a) In order to confirm that a tumor originally classified as a follicular variant of papillary cancer
is a NIFTP, it needs to be reread by a pathologist familiar with the new criteria. Some patients
will have invasive tumors, some may have classic
papillary cancer, and some may be NIFTP. The
diagnosis cannot be based on the original pathology report. Within a few years of diagnosis, the
original pathology tissue specimen blocks may
still be available for resectioning and re-evalua-
Table 2
Change in the Risk of Malignancy of TBSRTC Diagnostic Categories due to NIFTP Diagnosis
Cancer risk based on
TBSRTC 2007 (34)
Cancer risk based on post-2007
studies (24,27,28,35)
NIFTP effect on lowest to
highest cancer risk (24,28,30)
AUS/FLUS
(TBSRTC Cat-3)
5-15%
19-45%
15-30%
FN/SFN
(TBSRTC Cat-4)
15-30%
22-45%
10-37%
SM
(TBSRTC Cat-5)
60-75%
72-87%
46-68%
TBSRTC
Abbreviations: AUS/FLUS = atypia/follicular lesion of undetermined significance; Cat = category; FN/SFN = follicular neoplasm/suspicious for follicular neoplasm; NIFTP = noninvasive follicular thyroid neoplasm with papillary-like
nuclei; SM = suspicious for malignancy; TBSRTC = The Bethesda System for Reporting Thyroid Cytology.
Copyright © 2017 AACE
Managing Thyroid Tumors Diagnosed as NIFTP, Endocr Pract. 2017;23(No. 9) 1157
tion; however, there is no guarantee that the entire
tumor periphery was submitted for histopathologic evaluation to exclude invasion either into the
tumor capsule, surrounding thyroid, or vessels.
Thus, NIFTP should be viewed as a newly appreciated pathologic diagnosis that should not be
applied retrospectively.
(b) A benign clinical course after surgery with a low
serum thyroglobulin test and a negative neck
ultrasound is the most important outcome and
ultimately is more important than the pathologic
nomenclature. Moving forward, the AACE favors
careful education of pathologists and endocrinologists regarding the precise and prospective
diagnosis of NIFTP tumors to allow for unbiased
clinical and pathological study of the new category and its outcomes.
(2) “If my tumor is reclassified as NIFTP, do I still need
any long-term follow-up with an endocrinologist? “
(a) Since NIFTP cannot be diagnosed prior to surgery,
at a minimum, removal of at least half of the
thyroid is still required. Although many patients
may have had more aggressive surgery and/or
treated with radioiodine, these patients were treated according to the best knowledge available at
the time of their diagnosis. (b) Since NIFTP is a new diagnostic entity, at this
point what constitutes optimal follow-up is uncertain. In the absence of data, we are unable to
provide evidence-based recommendations. Until
data are available, each case should be considered
individually based on risk factors.
(3) “I was told I had cancer and now I am told I do not.
Who is responsible for my misdiagnosis?”
(a) Things change regularly in medicine as our
knowledge advances. At the time of the original treatment, no one (surgeon, endocrinologist, nuclear medicine physician) knew that the
follicular variant of PTC diagnosis was in question. You were treated appropriately according to
treatment guidelines at the time. In general, the
AACE does not advocate for retrospective review
of previously adjudicated EFVPTCs because:
(i) Proper reclassification demands retrieval
of the tumor block with repeat comprehensive sectioning to document the integrity of
surrounding tissue and tumor capsule and
the absence of papillary structures, lymphovascular invasion, papillary cancer variants,
psammoma bodies and tumor necrosis.
(ii) In many cases, the tumor block and appropriate slides are no longer available or interpretable.
(iii)In most cases, the clinical course over the
first 5 to 10 years after primary therapy is as
powerful a predictor of future tumor behavior
as the pathologist’s impression of the recut
tumor block.
(iv) Most thyroid cancer experts believe that
the new NIFTP criteria should optimally be
implemented in prospective rather than retrospective fashion to allow for unbiased clinical
and pathological study of the new category
and its outcomes.
CONCLUSION
Based on clinical cohort studies demonstrating favorable long-term outcomes, the Endocrine Pathology Society
Working Group has reclassified a noninvasive subset
of follicular variant of papillary cancers (noninvasive
EFVPTC) as NIFTP, thereby diminishing the psychologic
stigma of the word “cancer” for patients worldwide. It is
our hope that the new NIFTP classification will eventually
diminish clinical confusion among pathologists, endocrinologists, and endocrine surgeons and increase the use of
diagnostic (and therapeutic) thyroid lobectomy while diminishing thyroid hormone dependency and radioiodine use in
affected patients. The purpose of this communication is to
relay the clinical implications of the NIFTP thyroid tumor
reclassification to academic and community cytologists,
pathologists, endocrinologists, and endocrine surgeons
across the globe. Although we recognize that long-term
prospective NIFTP clinical outcome studies in academic
and community settings are needed to validate this change
in thyroid cancer diagnosis and treatment, we accept this
paradigm shift based on our current level of knowledge.
ACKNOWLEDGMENT
This manuscript was reviewed and approved by the
members of the AACE Thyroid Scientific committee and
Endocrine Surgery Scientific Committee.
DISCLOSURE
The authors have no multiplicity of interest to disclose.
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