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Please cite this article in press as: S.W. Lindley, et al., Communicating diagnostic uncertainty in surgical pathology reports: Disparitiesbetween sender and receiver, Pathol. – Res. Pract (2014), http://dx.doi.org/10.1016/j.prp.2014.04.006
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Pathology – Research and Practice xxx (2014) xxx–xxx
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Pathology – Research and Practice
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Original Article1
Communicating diagnostic uncertainty in surgical pathology reports:Disparities between sender and receiver
2
3
Sarah W. Lindley, Elizabeth M. Gillies, Lewis A. Hassell ∗Q14
Department of Pathology, The University of Oklahoma Health Sciences Center, BMSB 451, 940 Stanton L. Young Blvd, Oklahoma City, OK 73104, UnitedQ2States
5
6
7
a r t i c l e i n f o8
9
Article history:10
Received 23 October 201311
Received in revised form 13 February 201412
Accepted 15 April 201413
14
Keywords:15
Surgical pathology16
Communication17
Diagnostic Uncertainty18
a b s t r a c t
Surgical pathologists use a variety of phrases to communicate varying degrees of diagnostic certaintywhich have the potential to be interpreted differently than intended. This study sought to: (1) assessthe setting, varieties and frequency of use of phrases of diagnostic uncertainty in the diagnostic line ofsurgical pathology reports, (2) evaluate use of uncertainty expressions by experience and gender, (3)determine how these phrases are interpreted by clinicians and pathologists, and (4) assess solutions tothis communication problem. We evaluated 1500 surgical pathology reports to determine frequency ofuse of uncertainty terms, identified those most commonly used, and looked for variations in usage rateson the basis of case type, experience and gender. We surveyed 76 physicians at tumor boards who wereasked to assign a percentage of certainty to diagnoses containing expressions of uncertainty. We foundexpressions of uncertainty in 35% of diagnostic reports, with no statistically significant difference in usagebased on age or gender. We found wide variation in the percentage of certainty clinicians assigned tothe phrases studied. We conclude that non-standardized language used in the communication of diag-nostic uncertainty is a significant source of miscommunication, both amongst pathologists and betweenpathologists and clinicians.
© 2014 Published by Elsevier GmbH.
19
Background20
Communicating diagnostic uncertainty is an inherent part of all21
aspects of medicine. Pathology is presumed to be the final line in22
diagnosis, so when the pathologist expresses uncertainty in their23
diagnosis it could potentially lead to delayed treatment, repeat24
biopsy, and other interventions which increase medical expendi-25
tures and may negatively impact patient care.26
It is common practice in the pathology community to use27
phrases of uncertainty in the diagnostic line, most commonly when28
dealing with biopsy specimens. This may understandably be due to29
inadequate tissue, or extensive artifact that makes definite inter-30
pretation impossible. Other cited reasons for uncertainty include31
nonstandard histomorphology, ambiguous immunohistochemical32
stains, lack of clinical information, uncertain criteria in the liter-33
ature, lack of experience with the diagnosis, and hope (however34
unsubstantiated) to avoid legal liability for misdiagnosis.35
As pathologists we take pride in our linguistic acumen. When36
it comes to expression of uncertainty, pathologists are both very37
∗ Corresponding author. Tel.: +1 405 271 5653; fax: +1 4052712524.Q3E-mail addresses: [email protected], [email protected]
(L.A. Hassell).
particular and very inventive in the phrases that they use. A 2004 38
survey of sign-out practices of 96 veterinary pathologists found 39
they were using at least 68 unique terms to describe uncertainty [1]. 40
No comparable study has been published in the human pathology 41
literature. 42
Unsurprisingly, clinicians and others in the health professions 43
interpret and act upon these phrases in different ways based on 44
their understanding (or misunderstanding) of the intent of the 45
pathologist. To the pathologist “consistent with” and “worrisome 46
for” may be intended to mean different things and direct different 47
courses of action, perhaps expressing a graded continuum of diag- 48
nostic certainty corresponding to an internal scale on the behalf of 49
the observer; however if this difference is not being clearly per- 50
ceived by the clinicians, then we are doing a disservice, both to 51
ourselves and to our patients. This study sought to clarify and quan- 52
tify this potential gap between intent and perception and diagnostic 53
language, and to begin to seek means to narrow this chasm. 54
Methods 55
We determined the incidence of usage of phrases of diagnostic 56
uncertainty in our institution by reviewing 1500 sequential surgi- 57
cal pathology reports and tallying both the occurrence of phrases of 58
http://dx.doi.org/10.1016/j.prp.2014.04.0060344-0338/© 2014 Published by Elsevier GmbH.
Please cite this article in press as: S.W. Lindley, et al., Communicating diagnostic uncertainty in surgical pathology reports: Disparitiesbetween sender and receiver, Pathol. – Res. Pract (2014), http://dx.doi.org/10.1016/j.prp.2014.04.006
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2 S.W. Lindley et al. / Pathology – Research and Practice xxx (2014) xxx–xxx
uncertainty in the diagnostic line and the frequency of use of each59
term. These sequential reports were completed between August60
and October of 2011 (1000 reports) and April and May of 200961
(500 reports.) For the latter series of 500 cases, specifics of case62
type (biopsy, resection, etc.) category of question (neoplastic, med-63
ical) as well as additional determination as to gravity of issue64
was determined. Cases where use of the uncertainty phrase cen-65
tered around a peripheral or subclassification rather than the core66
(malignant/not-malignant) were also noted and quantitated.67
In order to investigate the trends of usage of uncertainty terms68
by practitioner, a separate series of 200 sequential reported cases69
for each of the 14 actively practicing surgical pathologists at our70
institution were evaluated. The incidence of use of uncertainty71
terms for each pathologist was calculated. This data was then used72
to assess the effect of age and gender.73
To assess how various phrases were interpreted by clini-74
cians, we administered an anonymous survey of attendees at75
multi-disciplinary tumor boards. The survey asked respondents to76
estimate the degree of certainty associated with eight diagnos-77
tic scenarios (Fig. 1). One diagnosis contained no expression of78
uncertainty while the other seven contained the following phrases:79
“cannot rule out”, “consistent with”, “highly suspicious”, “favor”,80
“indefinite for”, “suggestive of”, and “worrisome for”. The order of81
presentation of each phrase and the specific content or specimen82
type associated therewith was randomized between surveys. The83
clinical context of the diagnoses was also customized according to84
the specialty of the tumor board where the evaluation was per-85
formed. A total of 76 responses were received. Statistical analysis86
was by Student’s t-test and ANOVA. Subgroup analyses were per-87
formed based on level of training and clinical specialty (medical88
students, residents, fellows, attendings, medicine/medical subspe-89
cialists, pathologists/radiologists, and surgeons).90
Looking for viable solutions to reporting of uncertainty, we con-91
ducted a focus group by sending a more detailed survey to seven92
senior physicians in various departments (surgery, oncology, radi-93
ation oncology, gynecologic oncology, and otolaryngology). In this94
survey, respondents rank ordered eight phrases from least to most95
certain. We also asked respondents what their opinion for mov-96
ing forward to resolve this communication problem would be and97
assessed their response to examples of certain proposed solutions.98
Finally, to gain further input into possible solutions to this prob-99
lem, we held an open discussion with attendees at a short course100
at a national pathology meeting in fall 2012.101
Results102
Of 1500 surgical pathology reports, we found expressions of103
uncertainty in 529 (35%). The most commonly used phrase at our104
institution was “consistent with” (50%), while the other oft-used105
phrases included “suggestive of”, “worrisome for”, “cannot rule106
out”, “highly suspicious for”, “favor”, and “indefinite for” (Fig. 2). We107
found no statistically significant difference in incidence of uncer-108
tainty phrase usage by either age or gender (Fig. 3).109
Uncertainty phrases were used more often in biopsy cases (96110
of 149 incidences, 64%) than in resection cases. Most often these111
involved a question of neoplasic or pre-neoplastic (83 of 149, 56%)112
rather than medical (66 of 149, 44%) disease. About one-fifth (22%)113
of incident usage dealt with a “trivial” matter (e.g. “consistent114
with lipoma”, “favor ganglion cyst”) and a similar number (29 of115
149, 19%) dealt with a sub-classification issue (e.g. “serrated polyp,116
favor serrated adenoma” or “spindle cell sarcoma, consistent with117
undifferentiated pleomorphic sarcoma.”) Interestingly, only a small118
number of reports containing uncertainty phrases included a com-119
ment or clarifying note (20 of 149, 13%) to either explain the cause120
of the uncertainty or further direct management, and few if any121
Table 1Standard deviation of percent of perceived certainty, as a measure of the degreeof consensus regarding the level of certainty, for common uncertainty phrases insurgical pathology reports. Higher numbers indicate wider variability in the level ofunderstood certainty.
(a) Deviation by specialty
Medicine Pathologist/radiologist Surgeons
No phrase 30 6 13Consistent with 16 25 13Highly suspicious 26 19 27Worrisome for 22 23 22Favor 24 25 23Suggestive of 26 23 29Cannot rule out 31 21 30Indefinite for 21 24 31
(b) Deviation by level of training
Medical students Residents Fellows Attendings
No phrase 8.3 8.1 30 15Consistent with 16 21 8.9 24Highly suspicious 27 23 27 18Worrisome for 22 24 19 23Favor 10 23 23 24Suggestive of 22 26 23 25Cannot rule out 18 25 25 27Indefinite for 29 19 25 28
of these offered specific suggestions beyond “clinical correlation.” 122
Surprisingly, none of the 149 incident cases in our review of 500 123
sequential cases appeared to be due to ambiguous or inconclusive 124
special stains. 125
Clinical respondents demonstrated wide differences in the 126
assigned level of certainty perceived to be associated with hedge 127
words in the diagnosis, with overall certainty scores of 91% for no 128
waffle phrase, 79% for “consistent with”, 71% for “highly suspicious 129
for”, 61% for “worrisome for”, 73% for “favor”, 50% for “indefinite 130
for”, 62% for “suggestive of”, and 48% for “cannot rule out”. The 131
variations within the level of perceived certainty (representing a 132
measure of the clarity of the phrase) are quantified by the standard 133
deviations from the means (Table 1). The average percent certainty 134
of the various groups were compared, both by level of training 135
(Fig. 4) and by specialty (Fig. 5). ANOVA analysis of the certainty 136
per phrase yielded statistically significant differences between all 137
phrases except “indefinite for”, “suggestive of”, and “worrisome 138
for”. When these phrases were compared to each other, the means 139
were not statistically different (p = 0.05). 140
In our focused study of seven senior clinicians, we found marked 141
variability in the way that the clinicians ranked the certainty asso- 142
ciated with various phrases. We also found varied opinions as to 143
how we should resolve this communication problem from the dif- 144
ferent clinicians surveyed. Many of the free text comments we 145
received were illuminating, reflecting their own preferred manner 146
for resolving such issues. For example, one surgeon emphasized the 147
need to review the slide directly with the pathologist, or at a min- 148
imum have a direct phone conversation. Another emphasized that 149
the issue was not so much grading the degree of uncertainty as it 150
was determining the threshold to treat or pursue further diagnos- 151
tic evidence. Our initial survey also sought to assess which phrases 152
could be linked to various levels of action, but the data is not pre- 153
sented here. From the majority of comments in the focused survey, 154
only an unqualified diagnosis or the phrase “consistent with” were 155
deemed actionable for definitive therapy. 156
Discussion 157
In our review of surgical case reports we were surprised by 158
the 35% incidence of expression of diagnostic uncertainty. Some 159
Please cite this article in press as: S.W. Lindley, et al., Communicating diagnostic uncertainty in surgical pathology reports: Disparitiesbetween sender and receiver, Pathol. – Res. Pract (2014), http://dx.doi.org/10.1016/j.prp.2014.04.006
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S.W. Lindley et al. / Pathology – Research and Practice xxx (2014) xxx–xxx 3
Fig. 1. Example survey question.
of this represents common institutional or individual phraseol-160
ogy; e.g., “consistent with lipoma” and “focal changes suggestive161
of HPV cytopathic effect” and may not truly represent significant162
diagnostic uncertainty but are reflected in the overall incidence163
nonetheless. However, these kinds of trivial uses only accounted164
for 22% of cases. Also of note is that all of the pathologists in our165
institution used some phrases of uncertainty in the relatively small166
number of cases studied. This highlights the breadth of the prob-167
lem of expressing uncertainty in surgical pathology. The variation in168
usage between pathologists (ranging from less than 5% to over 35%)169
is also an issue of concern with regard to both quality and consis-170
tency of communication and may warrant monitoring. Expressing171
a level of uncertainty out of habit or extreme caution when none172
is truly present dilutes the value of the phrase when perspicuity173
is warranted or essential. Not surprisingly, biopsies accounted for174
nearly two-thirds of the instances of use, and the majority of these175
were questions of malignancy or dysplasia, areas well known to be176
prone to interpretive variability. Medical disorders however, also 177
accounted for a significant number of cases (44%) which seems to 178
be reflective of imperfect or overlapping histopathologic criteria for 179
entities such as chemical gastropathy, inflammatory bowel disease, 180
or the many inflammatory dermatoses. 181
We considered a number of potential reasons commonly 182
asserted to be associated with a hedged diagnosis. Analysis of 183
reporting pathologists’ usage of uncertainty phrases by both age 184
and gender revealed no statistically significant differences. This 185
refutes the notion that expression of uncertainty is correlated with 186
lack of experience or even more archaically, with the gender of 187
the pathologist. Our data does not support either of these ideas. 188
Other possible rationales for expressions of uncertainty in diag- 189
nostic lines may include contradictory or low probability staining 190
results, lack of or inconsistent clinical information, uncertain crite- 191
ria in the medical literature, quantity of sample or abnormality, and 192
possibly a desire to avoid legal liability for an over- or under-stated 193
62%38%
Frequency of Expressions of
Uncertainty
No
caveats
Waf�led50%
39%
Phrases Used Favor
Consistent
With
Suggestive of
Suspcious of
Cannot rule
out
Inde�inite for
Worrisome for
Fig. 2. Expression of uncertainty use at our institution.
Please cite this article in press as: S.W. Lindley, et al., Communicating diagnostic uncertainty in surgical pathology reports: Disparitiesbetween sender and receiver, Pathol. – Res. Pract (2014), http://dx.doi.org/10.1016/j.prp.2014.04.006
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52
41
13
35
10 9
17
26
10
29
37
68
20
33
0
10
20
30
40
50
60
70
80
60+60+60+60+30-4030-4030-4040-5040-5040-5040-5050-6050-6050-60
Num
ber o
f Waffl
e W
ords
Use
d pe
r 200
Sig
n-O
uts
Age
Fig. 3. Waffle word usage by age and gender.
Fig. 4. Average percent certainty by level of training.
Please cite this article in press as: S.W. Lindley, et al., Communicating diagnostic uncertainty in surgical pathology reports: Disparitiesbetween sender and receiver, Pathol. – Res. Pract (2014), http://dx.doi.org/10.1016/j.prp.2014.04.006
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S.W. Lindley et al. / Pathology – Research and Practice xxx (2014) xxx–xxx 5
Fig. 5. Average percent certainty by specialty.
diagnosis. These latter motives were not fully investigated in our194
study but may bear further scrutiny.195
While acknowledging that our method of sampling (written196
survey given at tumor boards) has limitations, including potential197
sample bias and response bias; we feel that this method was the198
most time and cost effective way to get a cross sectional study of199
clinicians at all levels of training and in a wide variety of specialties.200
Our questionnaire design incorporated elements of customization201
and presentation randomization to limit these biases.202
Overall, we found that the phrases “consistent with”, “highly203
suspicious”, and “favor” are perceived to be associated with more204
certainty in the diagnosis. The latter term is a surprise to be included205
in this group since it is regularly interpreted by pathologists as206
less certain than the other two and quite similar to “suggestive207
of”. But the surgical group ranked it more certain than “highly sus-208
picious” by almost 10 percentage points. The phrases “suggestive209
of”, “worrisome for”, and “indefinite for” were all less certain. The210
finding of no statistically significant difference in comparing the211
phrases “indefinite for”, “suggestive of”, and “worrisome for” across212
all groups of respondents tells us that these phrases are equiva-213
lent in terms of communicating uncertainty. So to the pathologist214
obsessing over a subtle internal rank order of phrases with which215
to exactly convey what they are seeing, for approximately 50–60%216
certainty in diagnosis, should probably relax and use one or any as217
our data shows them to communicate an equivalent message. This218
may be driven by the equivalent nature of the clinical response each219
phrase is likely to produce.220
To move toward at least a local solution to this problem, we221
conducted the focused survey of our senior clinicians. All but one222
of our respondents felt that only “carcinoma” and “consistent with223
carcinoma” were sufficient to treat. One respondent felt that even 224
“worrisome for carcinoma” was enough to treat given the right 225
clinical circumstance. 226
We posed some potential solutions to the focus group clinicians 227
at our institution and to a group of approximately 30 practic- 228
ing pathologists at a national forum on the topic. One option is 229
to develop a national consensus categorization with data-driven 230
guidance, similar to the Bethesda systems in cytology [2]. Less 231
ambitiously, we could develop a local departmental or institu- 232
tional consensus on usage communicated monolithically to users, 233
more gestalt-driven, perhaps based on cytology model with a tiered 234
system. So for example, a diagnosis of a malignancy without any 235
qualifiers would lead to definitive action; “suspicious for” or “con- 236
sistent with” would lead to definitive action if clinical story agrees; 237
and “atypical”, “favor”, “cannot rule out”, “suggestive of” would 238
be accepted to merit additional evaluation or follow-up. Alter- 239
nately, we propose an outcomes data driven solution based on 240
analysis of reports with various phrases from which a quantitative 241
qualifier could be appended (e.g., diagnoses containing the phrase 242
“suggestive of” are associated with an 80% probability of a posi- 243
tive diagnosis). An individually assigned, subjective quantization 244
of the intended degree of certainty (gestalt-based only) included 245
as a note or other element of the report itself might also close the 246
gap between sender and receiver, but would be subject to variable 247
usage and experience. The last and least rigorous option is to make 248
no reporting or usage change, but just build awareness amongst 249
pathologists and clinicians that use of these phrases leads to misun- 250
derstandings, and so might best trigger a phone call to the clinician 251
by the pathologist or vice versa to discuss the case and subsequent 252
actions. 253
Please cite this article in press as: S.W. Lindley, et al., Communicating diagnostic uncertainty in surgical pathology reports: Disparitiesbetween sender and receiver, Pathol. – Res. Pract (2014), http://dx.doi.org/10.1016/j.prp.2014.04.006
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Our focus group found elements of each of these proposed solu-254
tions attractive and useful, though they recognized the magnitude255
of the challenge in arriving at a data-driven solution given the num-256
ber and variety of causes for the problem, tissue sample types,257
locations and professional stakeholders potentially impacted. In258
presenting these various possible solutions to our forum on the259
topic at a national meeting, we again found no clear consensus on260
the best approach. Most importantly, this discussion highlighted261
the prevalence of this particular communication problem across262
all pathology practices.263
Some aspects of this issue have been previously studied in the264
British literature. Attanoos et al., studied phraseology in surgical265
reports and communication of uncertainty between surgeons and266
pathologists at the University Hospital Wales [3]. Galloway and267
Taiyeb examined the interpretation of phrases used to describe268
uncertainty amongst pathologists, other doctors, and medical stu-269
dents online and at the University College London Medical School270
[4]. In both of these studies, akin to our findings, there was wide271
variance in the interpretation of phrases between the groups stud-272
ied. They similarly concluded adoption of a limited number of273
descriptive phrases that are mutually understood and accepted by274
both pathologists and clinicians is needed to avoid ambiguity in275
surgical pathology reports. An additional study addressed the need276
for uniformity in reporting cancer for the British National Cancer277
Registry [5]. In his 2000 commentary on individuality in surgical278
pathology, Dr. Foucar aptly concluded, “. . .There is no place for the279
pathologist who expresses individuality by subjecting unsuspect-280
ing patients to uncontrolled diagnostic self-expression” [6].281
Although a clear consensus solution, either at our institution or282
among our colleagues elsewhere remains elusive; we have reached283
several important conclusions. Like the British studies, communica-284
tion of uncertainty indeed is a common practice and an unexamined285
source of possible medical error in the United States. We plan286
to study this possible relationship more fully. Our own anecdotal287
experience in tumor boards and an array of practice settings have288
provided several “near miss” examples, and more than a few need-289
less repeat biopsies or other procedures due to cautiously worded
reports with these phrases. Further study is needed to further refine 290
the specimens and diagnostic settings in which diagnostic uncer- 291
tainty is most commonly expressed in order to encourage improved 292
diagnostic criteria and provide better follow-up guidance when 293
such are not fully present and an uncertainty phrase mandated. 294
Additionally, it would be helpful to be able to calculate the possi- 295
ble cost to the health care system due to repeat biopsies in specific 296
cases. Secondly, action needs to be taken to address the issue of the 297
gap between uncertainty intention and perception at least locally 298
and preferably at a national level. An interesting trend appears to 299
be emerging from both our discussion at our institution and those 300
at the national meeting: more recently trained pathologists more 301
fully support national guidelines on terminology while more senior 302
pathologists tend to resist this loss of individuality in reporting. In 303
this and so many other aspects, it will be fascinating to see where 304
the new generations of pathologists take our field. Inasmuch as 305
interpersonal communication is a core competency for physicians 306
and training programs, the issue herein raised centers around a 307
critical practice skill for pathologists, and one where the data might 308
indicate we are not yet fully competent. In regards to clarity of com- 309
munication, our data suggests that moving toward uniformity both 310
in reporting style and language is the right direction. 311
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