A Review of Reporting Systems and Terminology for

Urine Cytology
Christopher L. Owens, MD
1
; Christopher J. VandenBussche, MD, PhD
2
;
Frances H. Burroughs, SCT(ASCP)
2
; and Dorothy L. Rosenthal, MD
2
Urine cytology continues to play an important role in the diagnosis and management of urothelial carcinoma, a common
cancer of adults with significant morbidity and mortality. Because of its high sensitivity for high-grade urothelial tumors,
including lesions that may be cystoscopically occult, urine cytology nicely compliments cystoscopic examination, a
method that detects most low-grade tumors. Over the decades, several reporting schemes for urine cytology have been
published in the literature, each of which has relative strengths and weaknesses. Unlike cervical cytology, there has not
been widespread acceptance and use of any particular reporting scheme for urine cytology studies. Thus, terminology
and criteria for urine cytology reporting are not uniform among pathologists, which can frustrate clinicians and hinders
interlaboratory comparisons. Cancer (Cancer Cytopathol) 2013;121:9-14. VC
2012 American Cancer Society.
KEY WORDS: urine cytology, reporting, terminology, urine reporting, template.
Urine cytology is an important test in the investigation of patients who are at risk for urothelial carcinoma
(UroCA) and in the surveillance of patients with UroCA, a common cancer of adults with significant mor-
tality. Advantages of urine cytology include ease of procurement, high sensitivity and specificity for high-
grade urothelial lesions that may be cystoscopically occult, ability to interrogate the entire urothelial tract,
and low cost. However, urine cytology has known limitations, including low sensitivity and low negative
predictive value in patients with low-grade urothelial tumors.
1,2
Fortunately low-grade papillary tumors
usually are detected easily by cytoscopy, so the clinical impact of this limitation is minimal. Another limita-
tion of urine cytology is the significant rate of equivocal or atypical results, which can lead to management
dilemmas for our clinical colleagues.
3,4
Over the years, several investigators have published classification schemes for urine cytology. The
schemes have evolved as the histopathologic classification of bladder lesions has changed, the understand-
ing of urine cytology and UroCA has increased, and the expectations of clinicians who send the urine for
study have changed. Establishing a clinically useful scheme for reporting urine cytology has been challeng-
ing, and some of the weaknesses of prior classification schemes include: lack of rigorous definition of
validated cytologic criteria for specific categories, lack of consensus for atypical categorization, and lack of
broad acceptance and use by the general pathology community. In this review article, we examine the
Received: August 19, 2012; Revised: September 13, 2012; Accepted: September 17, 2012
Published online November 28, 2012 in Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/cncy.21253, wileyonlinelibrary.com
Corresponding author: Christopher L. Owens, MD, Department of Pathology, UMass Memorial Medical Center, Three Biotech, One Innovation
Drive, Worcester, MA 01605; Fax: (508) 793-6110; christopher.owens@umassmemorial.org
1
Department of Pathology, University of Massachusetts Medical School, Worcester, Massachusetts.;
2
Department of Pathology, The Johns Hopkins
Hospital, Baltimore, Maryland
See related articles on pages 15-20 and 21-8, this issue.
Cancer Cytopathology January 2013 9
Review Article
evolution of classification schemes for urine cytology that
have been introduced in the literature and what has
prompted us to introduce a new scheme.
Early Work: George Papanicolaou
When Dr. Papanicolaou first began to consider applying
his smear technique, which had known utility in diagnos-
ing cervical carcinoma, to the study of urine sediments for
the diagnosis of bladder cancer, he initially was skeptical
of the endeavor. He admits in the introduction of one of
his early articles on this topic that he was quite pessimistic
regarding the projects outlook and was specifically con-
cerned about the potential for cellular degeneration and
its effects on accurate cytologic classification.
5
Working
with fellow pathologist Dr. Victor Marshall and urologist
Dr. Alexander Stevens, the team studied cytologic find-
ings from material obtained at New York Hospital and
Memorial Hospital of New York and correlated the find-
ings with histologic outcomes.
5,6
In their report on 240
cases, they noted that the potential problem with cellular
degeneration could be overcome with rapid fixation tech-
nique. More important, their results revealed that cytolog-
ically positive smears were highly predictive of UroCA on
biopsy.
Papanicolaou offered a classification scheme that
included 5 classes for reporting urine cytology ( Table 1).
Class 1 and 2 were essentially considered negative, Class 3
indicated suspicious for UroCA, and Class 4 and 5 indi-
cated positive for UroCA. The author observed that the
positive predictive value was 94.8% for positive cytology
(Class 4 or 5), 47.4% for suspicious cytology (Class 3),
and 7.4% for negative cytology (Class 1 or 2). That report
made several important observations and points that have
been confirmed by subsequent investigators. Recognizing
the limitations of urine cytology, the complimentary role
of urine cytology to other diagnostic techniques was
stressed. The ability of urine cytology to detect malig-
nancy before macroscopic disease also was noted by
describing a patient who was positive by urine cytology
and initially negative on biopsy. This particular patient
eventually was diagnosed with UroCA in a diverticulum.
Papanicolaou concluded that the tumor must have been
sufficiently small to be occult initially. This patient illus-
trated the complimentary role of cytology to direct exami-
nation for macroscopic disease, and this probably is the
first description of the so-called false false-positive phe-
nomena. Overall, the findings in Dr. Papanicolaous early
studies were tremendous and validated the role of urine
cytology in bladder cancer detection.
Although the categories for classification were
defined, the definitions or criteria for each category are
somewhat vague. He wrote that a conclusive positive cyto-
logic diagnosis should be based on clusters of malignant
cells as much as possible. The criterion for what is malig-
nant is not rigorously defined but features, including ani-
sonucleosis, anisocytosis, and crowding within fragments,
are mentioned. Criteria for suspicious (Class 3) were
abnormal cells but not pathognomonic for cancer and
mildly atypical (Class 2) were defined as atypical but not
with abnormal features.
Work by Leopold G. Koss
In a career spanning multiple decades and partially over-
lapping with that of Dr. Papanicolaou, Dr. Koss made in-
numerable contributions to the field of cytopathology and
urine cytology. His efforts resulted in numerous writings
with great impact, including the 2-volume Kosss Diagnos-
tic Cytopathology and Its Histologic Basis, now in its fifth
edition.
7
Koss sought to unite the fields of cytopathology
and histopathology, as the title implies, to the benefit of
both disciplines. Koss noted in a 2010 interview that,
early on, the fields were quite distinct and that patholo-
gists understanding was very vague about what cytopa-
thology had to offer.
8
He also opined in the same
interview that the class schemes preferred by Dr. Papani-
colaou for classifying cytologic studies were vague and
could be improved by basing the terminology on histo-
logic diagnoses (ie, suspicious for cancer is more informa-
tive than Class 3).
Accordingly, Kosss descriptions of the cytomorpho-
logic features in urine cytology were based on the histopa-
thologic classification of bladder cancer at the time (Table
2). The 1973 World Health Organization (WHO)
TABLE 1. Classification Scheme Proposed
by G. Papanicolaou
Class Definition
1 Absence of abnormal or atypical cells
2 Atypical cells present but without abnormal features
3 Cells with abnormal features but not
sufficiently pathognomonic
4 Fair number of pathognomonic cells and cell clusters
5 Large number of conclusive cells and cell clusters
Review Article
10 Cancer Cytopathology January 2013
classification system classified papillary tumors as either
benign papillomas or papillary carcinomas. Papillary car-
cinoma was divided into low-grade (grade 1), intermedi-
ate-grade (grade 2), and high-grade (grade 3) tumors,
depending on the architectural and nuclear abnormal-
ities.
9
Koss observed that low-grade tumors, including
papillomas and grade 1 papillary carcinomas, could not
be classified as malignant in urine cytology specimens.
7
He noted that papillary clusters and nuclear elongation
with pallisading were sometimes present in patients with
low-grade tumors but that the findings were not specific
and occurred in inflammatory conditions and in instru-
mented specimens.
10
Grade 2 and 3 papillary carcinomas
and nonpapillary carcinomas in situ, conversely, typically
shed clusters and individual cells sufficiently atypical to be
called positive in urine cytology studies. Koss observed
that cytomorphologic features supporting cancer included
nuclear hyperchromasia (most important), irregular
nuclear contours, abnormal chromatin texture (including
filamentous arrangements), and high cellularity.
Koss also addressed the issue of atypical urine cytol-
ogy specimens. He defined them as urothelial cells with
nuclear changes below the threshold of obvious cancer.
Atypical cells with hyperchromasia and predominantly
round or oval contours were classified as atypical 1 (ATY
1) cells, and those with hyperchromasia and nuclear mem-
brane abnormalities were classified as atypical 2 (ATY 2)
cells. The identification of a high number of ATY 2 cells
was commonly associated with cancer in his studies.
More Recent Classification Systems
Murphy and colleagues described cytomorphologic fea-
tures of UroCA and suggested a system of classification
for urine cytology in 1984 (Table 3).
11
In addition to
describing features of high-grade lesions, they described
criteria they found useful for identifying low-grade uro-
thelial tumors (grade 1 and some grade 2 lesions), includ-
ing papillary and loose clusters, increased cellularity,
eccentric nuclear location with more granular chromatin
pattern, 1 or 2 nuclear indentions, and lack of prominent
nucleoli. Those authors noted the difficulty in confidently
separating low-grade lesions from reactive changes and
conceded that, if a diagnosis of low-grade UroCA is ren-
dered regularly, then a modest false-positive rate must be
tolerated, and they suggested the cytologic diagnosis of
dysplasia as an acceptable alternative. Regarding the sepa-
ration of benign reactive cells from dysplasia, Murphy et
al reported that large cells with preserved nucleus-to-cyto-
plasm ratios, smooth nuclear contours, and vacuolated
cytoplasmsupported a benign process.
A few years later, in 1992, Ooms and Veldhuizen,
citing a lack of consensus on the cytologic criteria for cyto-
logic diagnosis of dysplasia proposed by Murphy, pub-
lished terminology for reporting urine cytology.
12
The
categories differed from Murphys by eliminating dyspla-
sia and by creating more categories for positive specimens
to follow the 1973 WHO nomenclature for histologic
typing of bladder cancer (Table 4). The criteria used for
classification were discussed but were not a major empha-
sis of their article, and they did not introduce performance
TABLE 2. Histopathologic Basis of Urine Cytology:
L. G. Koss
Histology Cytopathology
Benign Benign urothelial cells, few ATY 1 cells
Inflammatory conditions
and instrumented urine
Bland clusters/fragments; ATY 1 cells
Papilloma, grade 1
papillary carcinoma
Clusters, nuclear elongation
Grade 2 and 3 papillary
carcinoma, CIS
Malignant cells; numerous ATY 2 cells
Abbreviations: ATY 1, atypical cells with hyperchromasia and predominantly
round or oval contours; ATY 2, cells with hyperchromasia and nuclear
membrane abnormalities; CIS, carcinoma in situ.
TABLE 3. Classification Scheme Proposed by
Murphy
Negative/reactive
Dysplastic cells
Abnormal cells, suspicious for malignancy
Malignant tumor cells
Low-grade neoplasm
High-grade neoplasm
Squamous cell carcinoma
Undifferentiated malignant tumor
Nonepithelial neoplasm
TABLE 4. Classification Scheme Proposed by E. C.
Ooms
Negative cytology
Atypical cells, significance uncertain
Atypical cells, suspicious for malignancy
Neoplastic cells present
Grade 1 carcinoma
Grade 2 carcinoma
Grade 3 carcinoma
Carcinoma in-situ
Squamous cell carcinoma
Adenocarcinoma
Small cell carcinoma
Others
Urine Cytology Reporting and Terminology/Owens et al
Cancer Cytopathology January 2013 11
data (ie, predictive values, sensitivities, specificities) for
the various categories in their report. Within the papillary
urothelial tumor group, Ooms and Veldhuizen reported a
trend toward greater discohesion and, thus, more positive
single cells and greater nuclear atypia with increasing tu-
mor grade. Characteristics of (flat) carcinoma in situ
included single positive cells lacking papillary fragments
within a clean background.
Finally, in 2003 the Papanicolaou Society of Cyto-
pathology Task Force published recommendations for
diagnostic formatting and diagnostic categories for urine
cytology formatted in a similar fashion to the 2001 Be-
thesda System for reporting cervical cytology.
13
It is note-
worthy that these recommendations occurred after
publication of the 1998 WHO/International Society of
Urological Pathology (ISUP) changes to the histologic
classification of bladder tumors.
14
The new category of
papillary urothelial neoplasm of low malignant potential was
created by the 1998 WHO/ISUP system, to reflect the
low risk of bland papillary neoplasms that closely
resembled normal urothelium (encompassing most for-
mer grade 1 tumors) and to avoid stigmatizing patients
with a cancer label who harbored a low-risk lesion. The
remaining papillary carcinomas were classified by the
1998 WHO/ISUP either as high grade or low grade,
depending on the degree of architectural and cytologic
atypia. The Papanicolaou Society of Cytopathology Task
Force recommendations fell into line with the new histo-
logic characterization and simplified specimens that were
positive for UroCA into low-grade or high-grade UroCA
(Table 5). Their scheme included only 1 equivocal cate-
gory, simply called atypical urothelial cells. Those authors
noted that atypical urine cytology specimens are a prob-
lem and that further studies will be necessary to better
establish criteria for subclassifying atypical specimens.
Criteria useful for the classification of urine cytology as
positive are discussed but are not a major emphasis of their
report. The authors also addressed the incorporation of
ancillary studies, such as fluorescence in situ hybridiza-
tion, into urine cytology reporting, reflecting the emer-
gence of adjunctive studies in urine cytology that
continues today. Table 6 compares the cytologic
classification schemes of urine cytology discussed above
and the histologic classification of papillary bladder
tumors.
Contemporary Studies of Urine Cytology
More recently, several studies have focused on atypical
urine cytology in efforts to define the clinical significance
of this category and to identify cytomorphologic features
with high risk for UroCA and those associated with
benign outcomes. In each of these studies, the criteria for
atypical is unique and may not be the same as the criteria
used by another investigator. Not surprisingly, widely di-
vergent results have been observed in histologic outcome
studies of atypical urine cytology specimens. Some studies
have demonstrated significantly higher rates of UroCA af-
ter a finding of atypical urine cytology compared with a
negative finding,
3,15
and others have observed no signifi-
cant difference in rates of UroCA when comparing atypi-
cal versus benign urine cytology.
16
It is clear from these studies that the atypical cate-
gory is not well defined in the literature; studies examin-
ing outcomes of atypical urine cytology are difficult to
compare, and the results probably are not generalizable.
Renshaw addressed atypical urine cytology in a study to
determine which cytologic features were most helpful to
better classify such a specimen as either suspicious for
UroCA or benign.
4
He also noted the heterogeneity of the
category and the tendency for over use. He identified 7
common patterns and reported that diffuse, significant
urothelial atypia, defined as increased nucleus-to-cyto-
plasm ratios and irregular nuclear contours, was a com-
mon pattern observed in low-grade UroCA and that
diffuse, dark chromatin in a cell with intact nuclear mem-
branes was a dangerous finding that was associated most
TABLE 5. Papanicolaou Society of Cytopathology
Practice Guidelines Task Force
I. Adequacy statement
II. General categorization
Negative for epithelial cell abnormality
Epithelial cell abnormality present (see Descriptive Diagnosis)
III. Descriptive diagnosis
Negative for epithelial cell abnormality
Infectious agents (bacterial organisms, fungal organisms, viral
changes)
Nonspecific inflammatory changes
Cellular changes associated with chemotherapy or radiation
Epithelial cell abnormalities
Atypical urothelial cells (see Comments)
a
Low-grade urothelial carcinoma
High-grade urothelial carcinoma
Squamous cell carcinoma
Adenocarcinoma
IV. Others
A comments section is included at the discretion of the cytopathologist.
Findings from ancillary studies can be incorporated in this section.
Review Article
12 Cancer Cytopathology January 2013
often with high-grade UroCA. Renshaw reported that
cells with this coal-black type of chromatin, even if rare,
should be reported as at least suspicious for UroCA to
ensure adequate follow-up.
In clinical practice, most practicing cytopathologists
will separate atypical urines into 2 general categories: sus-
picious for UroCA and atypical not otherwise specified.
The second category, which is reserved for specimens that
appear to be abnormal but fall short of suspicious. There
is also debate regarding whether the finding of cytologi-
cally bland urothelial fragments in a noninstrumented
specimen justifies an atypical classification. Some author-
ities on the subject believe that this finding indicates an
increased risk of low-grade urothelial neoplasia, whereas
others maintain that this finding can safely be ignored.
17,18
Others believe that the character of the fragment is impor-
tant: Smooth contours at the edge of the fragment, cellular
crowding within the fragment, and lack of maturation
would favor a low-grade urothelial neoplasm.
19
Those
who believe that a urothelial fragment warrants an atypical
label would typically sign out such a case as in the atypical
not otherwise specified category or would create a third
atypical category just for this scenario. Many laboratories
have even come up with their own specific explanatory
note indicating the uncertainty of a bland urothelial frag-
ment and the differential diagnosis.
There has also been a recent explosion of literature
investigating ancillary methods to study urine for the detec-
tion of UroCA as either an adjunct to or a replacement for
urine cytology. Extensive exploration of this topic is beyond
the scope of the current report, but several review articles
have been written on these techniques for interested read-
ers.
2022
UroCA is the most expensive cancer to treat from
diagnosis to death; therefore, scrutiny of the cost-to-benefit
ratio of any study used for diagnosis or monitoring will be
important in the future.
23
We are not convinced that fluo-
rescence in situ hybridization or any of the other commer-
cially available studies add substantially to the detection or
surveillance of UroCA over what can be accomplished with
cystoscopic examination and urine cytology.
In summary, over the decades, several classification
schemes for reporting urine cytology have been proposed
that have evolved in accordance with the histologic classi-
fication of bladder tumors and as limitations to urine cy-
tology have become apparent. Unlike the case with
cervical cytology reporting, a single standard and widely
accepted reporting system has not emerged. Thus, the
diagnostic categories for reporting urine cytology are vari-
able among different laboratories, reflecting tendencies of
individual cytopathologists and feedback from clinicians.
More important, different laboratories place various levels
of importance on cytomorphologic features that are used
TABLE 6. Comparison of Classification Schemes for Urine Cytology and Histologic Classification of Papillary
Urothelial Tumors
Cytologic Classification Histologic Classification
Papanicolaou
1947
5
(Papanicolaou
Classification
System) Koss 1985
10
Murphy
1984
11
Ooms &
Veldhuizen
1993
12
Layfield
et al 2004
13
(Papanicolaou
Society of
Cytopathology)
Hopkins
Template
a
Mostofi & Torloni
1973
9
(WHO)
Epstein 1998
14
(WHO/ISUP)
I Benign cells,
ATY 1 cells,
few clusters
Negative Negative Negative NUAM Papilloma Papilloma
II TCC, grade 1 PUNLMP
LGUC
III Clusters, nuclear
elongation,
few ATY 2 cells
Dysplastic
cells
Atypical,
significance
uncertain
Atypical
urothelial cells
AUC-US TCC, grade 2
Suspicious Suspicious AUC-H
IV Malignant
tumor cells,
many ATY
2 cells
Malignant
cells
Neoplastic
cells present
Urothelial
carcinoma
Urothelial
carcinoma
HGUC
V
TCC, grade 3
Abbreviations: ATY 1, atypical cells with hyperchromasia and predominantly round or oval contours; ATY 2, cells with hyperchromasia and nuclear membrane abnor-
malities; AUC-H, atypical urothelial cells cannot exclude high-grade urothelial carcinoma; AUC-US, atypical urothelial cells of uncertain significance; HGUC; high-
grade papillary urothelial carcinoma; ISUP, International Society of Urological Pathology; LGUC, low-grade papillary urothelial carcinoma; NUAM, no urothelial atypia
or dysplasia identified; PUNLMP, papillary urothelial malignancy of uncertain malignant potential; TCC, transitional cell carcinoma; WHO, World Health Organization.
See Table 7.
Urine Cytology Reporting and Terminology/Owens et al
Cancer Cytopathology January 2013 13
to categorize urine cytology. Therefore, what 1 observer
may call atypical not further specified, another observer
may classify as suspicious for UroCA, cytodiagnoses that
are quite different to the clinician. This current state of
urine cytology reporting can be frustrating to our clinical
colleagues and, without improvement, jeopardizes the
confidence of clinicians and continued use of the test.
It is with all of this in mind that we offer the Johns
Hopkins Hospital Template for Reporting Urine Cytology
(Table 7), based on blinded analyses of several cytomorpho-
logic criteria. Our hope is to offer a system with well
defined and clinically relevant diagnostic categories to pro-
vide a common language for reporting urine cytology. We
stress that the cytologic criteria are not unique and have
been offered by previous investigators as useful for assigning
risk to urine cytology (and we are grateful for the prior
efforts). This review highlights the evolution of terminology
but also demonstrates that we have been observing the same
things for years, only using different names. Recall Dr. Pa-
panicolaou noticing abnormal but not pathognomonic or a
Class 3 smear, Dr. Koss noting that ATY 2 cells are suspi-
cious for carcinoma, more contemporary cytopathologists
and their coy cells, or Dr. Renshaw passionately writing to
not dismiss even a rare cell with a dark lump-of-coal chro-
matin pattern. It is time we all got on the same page and
used a single reporting system. We hope that the template
will be useful and that it will be critically assessed by practic-
ing cytopathologists so that it may be improved upon.
FUNDING SOURCES
No specific funding was disclosed.
CONFLICT OF INTEREST DISCLOSURES
The authors made no disclosures.
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TABLE 7. Diagnostic Categories of the Hopkins
Template for Urine Cytology Samples
No urothelial atypia or malignancy identified (NUAM)
Urothelial carcinoma (specify)
High-grade (HGUC)
Low-grade (LGUC)
Atypical urothelial cells of uncertain significance (AUC-US)
Atypical urothelial cells, cannot exclude HGUC (AUC-H)]
Other
Review Article
14 Cancer Cytopathology January 2013