Surgical Pathology_Second Reviews_Institutional Reviews_Audits_and Correlations

Surgical Pathology—Second Reviews, Institutional Reviews, Audits, and Correlations What’s Out There? Error or Diagnostic Variation?

William J. Frable, MD

● Context.—A variety of methodologies have been used to report error rates in surgical pathology within the peerreviewed medical literature. The media has selectively and superficially reported these error rates creating a climate of disinformation between physicians and the public.

Objectives.—To review the medical literature on diagnostic error in surgical pathology and summarize and compare these data with selected reports in the print and broadcast media.

Design.—A search of the medical literature from the National Library of Medicine database using the heading ‘‘Error and Pathology Diagnosis.’’

Results.—Three thousand nine hundred ninety-two citations were found, of which 83 directly measured in some manner errors in surgical and cytopathology. Major error rates ranged from 1.5% to 5.7% globally for institutional consults. Error rates were less, 0.26% to 1.2% for global in-house prospective review and 4.0% for in-house and retrospective blinded review. Error rates also varied by anatomic site: skin, institutional consult, 1.4%; prostate, institutional consult, 0.5%; and thyroid, institutional consult,

7.0%. Error rates reported in citations used by the Wall Street Journal were as follows: prostate, Gleason score changed by 1 point, 44% and resultant change in treatment for prostate cancer, 10%; for breast, altered lumpectomy or mastectomy plan, 8%; and diagnosis changed for thyroid lesions, 18%. Errors in second opinion on breast lesions (single pathologist author for the study) fall within the range of global reviews. Errors for second opinions on prostate cancer were principally 81% upgrades in Gleason score for prostate core needle biopsies. However, this resulted in an upgrade of patient risk category in only 10.8% of patients. Data for the article on change in diagnosis of thyroid lesions were incomplete. There appeared to be 3 significant diagnostic errors (4.5%).

Conclusions.—Pathology is not immune to the power of the media to create concern about accuracy of diagnosis in surgical pathology and cytopathology. Detailed analysis of the medical literature cited by the media determines that painting the big picture and hitting the highlights can be profoundly misleading.

(Arch Pathol Lab Med. 2006;130:620–625)

I

shadowed by social security, judicial appointments, and the war on terrorism.

Has pathology been unaware of errors? Certainly not.

A search of National Library of Medicine reference listings using ‘‘Error and Pathology Diagnosis’’ found 3992 citations, the first in 1966. While not all of these publications are directly related to surgical pathology or cytopathology, 83 of them seem to be relevant to the discussion of diagnostic error or variation. An additional incentive for pathology to examine errors may be the increasing awareness of malpractice involving pathologists, which became apparent in the early 1990s with high-profile cases of alleged false-negative readings of Papanicolaou tests.

The first allegations against pathology that came to my attention were in an article by Tara Parker-Pope, entitled ‘‘Risk of Error May Justify Second Opinion on Pathology Reports,’’ which appeared in the Wall Street Journal in April 2001.4 Ms Pope, a writer for the Wall Street Journal, has authored a number of articles on health issues in her column, ‘‘Health Journal.’’ The 2001 column stated that review of pathology slides on patients referred to Johns Hopkins Hospital revealed serious errors in 1.4% of cases.5 In reference to prostate needle biopsies, Pope cited Epstein who reported that 20% of the time mistakes were made

n recent years there has been an increasing awareness of patient safety issues in medicine. The comprehensive and far-reaching Institute of Medicine report, To Err Is Human: Building a Safer Health Care System, published in 2000, gained widespread media attention.1 Thoughtful critique of that report essentially went unnoticed by the lay press.2,3 Regardless of whether one believes the data and the report, certainly public awareness was heightened and the medical profession began to take steps to address perceived problems. Tort reform was a significant campaign issue in the 2004 election but appears to be currently over-

Accepted for publication January 3, 2006.

From the Department of Pathology, Virginia Commonwealth University, Medical College of Virginia, Richmond.

The author has no relevant financial interest in the products or companies described in this article.

Presented in part at the annual meeting of the Association of Directors of Anatomic and Surgical Pathology, San Antonio, Tex, February 26, 2005, as part of a symposium entitled ‘‘Error Reduction and Critical Values in Anatomic Pathology.’’

Reprints: William J. Frable, MD, Department of Pathology, Virginia Commonwealth University Medical Center, 1200 E Marshall St, Richmond, VA 23298-0115 (e-mail: wfrable@vcu.edu).

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in staging and grading. On May 8, 2001, ABC World News Tonight, picking up on the Wall Street Journal article, aired a short segment entitled ‘‘Closer Look,’’ focusing on the error rate of 20%.

The College of American Pathologists responded in a letter from the president at that time, Paul Bachner, MD, to Mary Harris, producer of ABC World News Tonight. 6 Some of that letter is reproduced as follows: 1. ‘‘It is my understanding that ABC contacted the College of American Pathologists (CAP) requesting the name of an expert in this area of pathology and that we provided the name of Dr. Patrick Fitzgibbons, the chairman of our Surgical Pathology Committee. I have been informed that Dr. Fitzgibbons was not contacted.’’

2. ‘‘I am very surprised that ABC did not avail itself of the opportunity to speak with a representative of American pathology.’’

3. ‘‘Specifically, the cases that have been reported by Dr. Epstein may represent an unusually complex sample of patients referred to a tertiary care medical center and are not representative of the very large number of cases that are seen and accurately diagnosed by American Pathologists. Not stated by anyone last Tuesday night, including Dr. Epstein, who is a well respected expert in the pathology of the prostate gland, is that over 98 percent of the original diagnoses in Dr. Epstein’s published paper were verified by the ‘second opinion’ review. Surely responsible journalism would require that fact to have been disclosed to the viewing audience!’’

4. ‘‘The CAP encourages patients who are concerned about the accuracy and reliability of their pathology diagnoses to discuss their concerns with their physicians. This discussion should include basic information about the laboratory and the pathologist, accreditation status of the laboratory, the physician’s previous experience with the laboratory and the pathologist, and perhaps most important, whether the physician has the opportunity to communicate directly with the pathologist about the patient and the patient’s specific medical circumstances.’’

Dr Epstein clarified his comments in a letter published in CAP Today, May 20, 2001, as follows: I would like to clarify my comments on a recent ABC nightly news program regarding second opinions in surgical pathology.

I was interviewed for over three hours of which they selected about 20 seconds of sound bites. Throughout the interview I repeatedly stressed that the vast majority of pathologists are excellent physicians and that the diagnoses they render are correct.

However, a minority of cases benefit from a second opinion, especially in select problematic areas in pathology. It was never my intent to malign general pathologists, but rather to sensitize patients that pathologists exist, that certain diagnoses are difficult, and that in a minority of cases, patient management benefits from a second opinion. I am sorry that the news report did not fully express my opinions.7

CAP Today, in its July 2001 issue, featured a lengthy discussion of second opinions in a very thoughtful article authored by Karen Titus, ‘‘No Rights, No Wrongs in Second Opinions.’’ 8 As well as commentary and discussion from well-known pathologists, comments were reported from Ms Pope and other patient advocates, as follows.

1. Jerome Groopman, MD, in the July 2001 issue of Prevention stated, ‘‘In many cases pathologists disagree, or test results may not be reliable.’’

2. According to Charles Inlander, president of The Peoples Medical Society, syndicated columnist and frequently heard on National Public Radio, ‘‘One out of every five diagnostic first opinions are [stet] not confirmed by second opinions.’’ He added that up to 80% of second opinions don’t get confirmation. He also noted that at least one Arch Pathol Lab Med—Vol 130, May 2006

Table 1. Data Cited by Tara Parker-Pope in Her Wall Street Journal Column (2005) Johns Hopkins Hospital reports—serious errors Cancer not present or wrong type of cancer Female reproductive tract Skin cancer Prostate staging and grading

5.1% 2.9% 20.0%

Dana Farber Cancer Institute—significantly high error in prostate Gleason score changed by at least 1 point Change in treatment

44.0% 10.0%

Northwestern University Medical Center study 2002—340 breast cancer patients Altered lumpectomy or mastectomy plans

8.0%

St James University Hospital, London, England—66 cases of thyroid cancer referrals Diagnosis changed

1.4% of cases

18.0%

pathologist’s research ‘‘has shown some of the terrible work that’s done in pathology, particularly oncology.’’

3. Concerning Ms Pope, Ms Titus reports in her 2001 article in CAP Today: ‘‘She’s [Ms Pope] familiar with complaints that consumer medical stories omit critical information, but says ‘I [Ms Pope] am not writing a textbook.’ ’’ Ms Pope goes on to say, ‘‘My goal is to give patients the highlights, the big points that will prompt them to have a conversation with a doctor on the subject. I leave it to the medical profession to help patients decide what is best for them. . . . Patients want information, even if in a condensed version, because it is often more than their doctor will give them.’’

Unfortunately, none of this dialogue appeared in the public news—printed or electronic. Ms Pope surfaced again in her Wall Street Journal column in February 2005 in a report titled ‘‘Why It’s Hard to Get a Second Opinion (And How to Make Sure You Get One).’’ 9 In a sidebar to the article, she reiterated the 20% error rate for surgical pathology. Since Ms Pope provided an e-mail address, I contacted her requesting the specific peer-reviewed articles in the medical literature on which she based her conclusions about errors in surgical pathology. No response occurred until a second e-mail was sent reiterating the request and specifying that her lack of response would be noted at a presentation before the largest and most prestigious pathology society in North America. That resulted in an immediate response. Several studies were cited, though the specific references were not provided. However, there was enough information for me to track them down and analyze them. Table 1 summarizes these studies as they appeared in the 2005 Wall Street Journal article.10–12 Summaries of a number of references with respect to errors in surgical pathology are presented in Table 2.5,13–26 Data are presented for major errors as stated by the various authors to have a significant impact on patient care.

The results obviously vary with respect to review as a referral generally to a major center prior to therapy or a second opinion versus an in-house self-audit. The latter also vary depending on a review of biopsies only versus all types of cases, 1.2% compared to 4.0%. Variation by anatomic site is also not unexpected, some sites and cases, ADASP Symposium—Frable 621

Table 2. Reported Rates of Major Errors in Surgical Pathology Global and Selected Sites5,13–26 Type of Review

Range of Major Error, %

Global Institutional consults* In-house prospective In-house retrospective blinded†

Type of Change

Grade of tumor not included

1.4–5.7 5,13,14 0.26–1.2 15,16 4.017–19

Organ/anatomic site: institutional Skin 1.420,22 Prostate 0.521 Head and neck 7.024 Thyroid 7.524 Gastrointestinal-Liver 6.8–7.5 25 Gynecologic 2.026 * Case referred to institution for review prior to therapy and/or second opinion. † Percentage was 1.2% for biopsies only.

Table 3. Summary Data From Pathology Second Opinion in a 4-Year Study of Breast Cancer11 No. of patients No. of breast cancers

340 346

Pathology second opinion results No change in pathology or prognosis, % Some change, % Major change: altered surgical therapy, % Prognostic factors added, %

20 80 7.8 40.0

Table 4. Major Changes in Pathology Diagnosis After Second Opinion in 340 Patients With Breast Cancer11* Initial Diagnosis

Table 5. Minor Changes in Diagnosis After Second Opinion Review in 340 Patients With Breast Cancer11

Second Opinion Diagnosis

No. of Cases

% Total Cases

DCIS Benign 1 0.3 DCIS Invasive cancer 6 1.7 Invasive Cancer DCIS 7 2.0 Margins positive Margins negative 10 4.1 Margins negative Margins positive 6 2.5 * Reprinted with permission from Springer Science and Business Media. DCIS indicates ductal carcinoma in situ.

pigmented skin lesions and needle core biopsies of breast and prostate being both high profile and problematic.20–23 The 7.0% rate for head and neck cases, with the exception of thyroid, is somewhat surprising, as referrals for major therapy requiring review would be expected to be the common head and neck cancers.24 A review was then made of the specific references sited

by Ms Pope in her Wall Street Journal column in support of the high error rate in surgical pathology. Table 3 summarizes the findings in the article by Staradub et al11 for breast cancer, a second opinion review of pathology prior to a discussion and/or implementation of therapy.

Analysis shows that there was 1 pathologist of the 5 authors of this study. Presumably that pathologist, Elizabeth L. Wiley, MD, rendered all of the second opinions.

Table 4 presents a summary of the major changes in pathology as documented in the article. The results presented fall within the range of global reviews of institutional consults or second opinions. Additional commentary in the article is revealing. For example, in the discussion of ductal carcinoma in situ versus invasive breast cancer, it is noted that in 5 cases there was diagnostic uncertainty 622 Arch Pathol Lab Med—Vol 130, May 2006

Change between grade 1 and other grades Change in subtype, to or from favorable Addition or deletion of DCIS from invasive cancer * DCIS indicates ductal carcinoma in situ.

Diagnosis*

% of Cases

DCIS Invasive DCIS Invasive DCIS

57 38 11.1 7.4 44.4 17.8

both on initial and second opinion review. The pathologist believed that 2 cases were invasive where this finding was not definitively reported initially, while 2 additional cases had the possibility of invasion raised on second opinion but not definitely reported. One case was changed on review from invasion to ductal carcinoma in situ with possible invasion. No additional comments were made on change in margin status.

That agreement is not universal among expert breast pathologists has been documented in at least 2 articles.27,28 The first appeared in 1991 and noted that in 17 borderline epithelial proliferations of the breast reviewed by 5 expert pathologists, 4 of 5 pathologists agreed on only 3 of the cases. Diagnoses in 6 of the cases ranged from hyperplasia to carcinoma in situ.27 Using standardized criteria and consensus study of 24 ductal proliferative lesions of the breast, 6 expert breast pathologists reached complete agreement in 58% of the cases, while 4 of the 6 pathologists agreed in 92% of the cases.28 With respect to microscopic invasion, Rosen devotes 5 pages and 11 illustrations to the discussion of microscopic invasion in breast cancer and notes as follows: ‘‘The diagnosis of microinvasion is also confounded in some instances by the capacity of invasive carcinoma to assume a growth pattern that simulates intraductal carcinoma.’’ 29 Table 5 summarizes what were considered to be minor changes in diagnosis from the paper by Staradub et al.11 Since most of the items listed in Table 5 may represent subjective and subtle interpretations, it would seem logical to consider the expertise of the pathologist involved. A search of the medical literature using PubMed for ‘‘E. L. Wiley’’ retrieved 41 articles in peer-reviewed journals. A review of those articles, while quite scholarly, did not uncover any article devoted to subtyping or grading of breast cancer or evaluation of and criteria for margin status. In this respect, a quotation from the Staradub article is of some importance: ‘‘We believe that an in house second opinion offers the surgeon the advantage of a consultation from a pathologist whose diagnostic criteria are familiar to the surgeon [emphasis added] and who is accessible for case review.’’ 11 A most interesting article published by Wiley and Keh,30 regarding diagnostic discrepancies in breast cancer specimens subjected to gross examination, is of significant interest. This was a study from Wiley’s institution.

The findings are summarized in Table 6. Residual tissue was available for examination in 1120 cases. Reexamination demonstrated major discrepancies in 5% of cases, 8 additional positive lymph nodes, and 37 missed cancers.

The second article cited by Ms Pope is a study of second review (institutional consult) of prostate core needle biopsies by Nguyen et al,10 and the impact of treatment ADASP Symposium—Frable

Table 6. Gross Evaluation of Breast Specimens: Major Changes in Diagnosis on Review30 Breast specimens submitted for a 2-y study using residual tissue Mastectomies 520 Wire local excisions 143 Lumpectomies 156 Mammoplasties 301 Total No. 1120 Major discrepancies Additional positive lymph nodes Missed cancers Minor discrepancies

5% of cases 8 37

Total No. of cases reviewed No. (%) of cases given a different pathologic diagnosis No. of cases changed from malignant to benign No. of cases changed from benign to malignant No. of cases in which prognosis improved after pathology review No. of cases in which prognosis worsened after pathology review

66 12 (18) 2 2 4 8

6% of cases

Table 7. Data Cited by Tara Parker-Pope in Her Wall Street Journal Column (2005): Prostate Cancer Second Opinion Errors10 No. of needle biopsies analyzed in a 3-y period Gleason score changed at least 1 point, % Upgrades, % Upgrades of patient risk category, % Downgrades of patient risk category, %

602 44 81 10.8 3.4

based on that review. The findings of this study are summarized in Table 7.10 Underscoring by community hospital pathologists using the Gleason system is clearly an identified problem. The authors’ point was that underscoring would lead to underevaluation of risk of the use of monotherapy (ie, surgery or radiation) versus multimodality therapy. Carlson and colleagues had previously reported this problem, which to some degree was featured in the original Wall Street Journal article by Pope.31,32 If one studies the monograph by Epstein and Yang, the following quotation is of interest: ‘‘We do not diagnose Gleason score 2 through 4 on needle biopsy.’’ 33(p155) A prominent surgical pathologist from another academic institution handling a large volume of prostate needle biopsies has stated, ‘‘We never diagnosis anything less than Gleason score 6 (3⫹3)’’ (R. Kempson, oral communication, January 1998).

I have participated in several pathology practice audits in which slides and reports are reviewed for a significant sample of cases. Underscoring of prostate needle core biopsies is a consistent finding when cancer is present.

Many of these cases appear to be small foci of a few glands for which the differential lies between small atypical glandular proliferation and cancer. Immunohistochemical studies for high-molecular-weight cytokeratin may have been performed to sort out these cases, but if a decision is made that cancer is present, there is a distinct tendency to score it as a 2 or 1 pattern, based on its small size rather than circumscription, which cannot be determined on a needle core biopsy.

Recognizing the problem of accurate Gleason scoring, a Web-based tutorial was developed by pathologists at Johns Hopkins and can be found at www.pathology.jhu.edu/ prostate.34 Interestingly, in the tutorial an image of a Gleason pattern 2 is shown in a needle biopsy. When one takes the examination after completing the tutorial, this same image is shown and scored as a 3⫹3 ⫽ 6.

For the 3 pathologist authors of the article by Nguyen et al,10 a search was conducted using the PubMed (National Library of Medicine) database to obtain all of their published work. Titles and abstracts were reviewed to find Arch Pathol Lab Med—Vol 130, May 2006

Table 8. Pathology Second Opinion in Thyroid Cases12

articles on grading of prostate cancer. A total of 402 papers were found for the 3 pathologists. Of those, 1 was devoted to the grading of prostate cancer.35 The conclusion of the article by Nguyen et al is also noteworthy: ‘‘The question, however, of whether combined modality therapy has a survival benefit over monotherapy in intermediate and high risk patients awaits the results of completed randomized clinical trials.’’ 10 The third article used by Ms Pope in her expose of errors in surgical pathology, which discussed second opinions in thyroid pathology, is more difficult to analyze, as the information within the text and tables is not entirely complete. The findings from the cases reported are summarized in Table 8.12 What Ms Pope failed to mention in her article is that 17 of the 66 cases were referred by general pathologists for a second opinion: 15 for confirmation of the original diagnosis and 2 with a differential diagnosis. There was also some significant pathology second opinion commentary that was not addressed by the Wall Street Journal article. There were 3 cases of follicular carcinoma in which the difference in opinion turned on minimally invasive versus widely invasive. There were 2 cases in which the difference was Hu¨rthle (oncocytic) adenoma versus carcinoma.

With regard to vessel invasion, a very well-known thyroid pathology expert believes that the criteria of 4-vessel invasion for determining widely invasive follicular carcinoma as the minimum is arbitrary and unproven.36 In the third series fascicle of the Armed Forces of Pathology, Tumors of the Thyroid, 3 pages and 11 illustrations are devoted to the topic of capsular and vascular invasion in thyroid carcinoma.37 Cell type was also an issue in the article by Hamady et al12 cited

by Ms Pope. A difference of opinion occurred for 3 cases, 2 follicular versus papillary and 1 follicular carcinoma versus Hu¨rthle cell (oncocytic) carcinoma. It is doubtful that the change in cell type has any impact on prognosis, and there is no difference in prognosis between papillary carcinoma if it was encapsulated (information not reported in the article) versus follicular adenoma.

From the data that are available in the article by Hamady et al,12 it would seem that there are 3 (4.5%) significant diagnostic errors out of the 66 cases reviewed. One is a diagnosis of follicular carcinoma with a review opinion diagnosis of normal. In that case, one would have to ask whether a complete set of slides or slides from the correctly identified patient were sent, items not addressed by the authors. In 2 others, the difference in opinion seems to be upstaging of papillary carcinoma, but the specifics leading to that conclusion are not discussed. All other variations reported in this study appear to be diagnostic variance dependent on interpretation of subjective criteria. In searching for the expertise of the pathologist authors of ADASP Symposium—Frable 623

the Hamady article, the total number of publications for the 2 pathologists were 85 peer-reviewed papers. None could be found that addressed histologic type, criteria of vascular invasion, or the criteria of minimally invasive versus widely invasive thyroid carcinoma.

COMMENT The power of the media to influence public opinion and create concern is remarkably strong. Medicine and pathology are not immune. Painting the big picture and hitting the highlights can be profoundly misleading, as this analysis suggests. Undoing inaccurate and sensational reporting with careful analysis can be extremely difficult and is generally lost on the public and the press. As Foucar38 has noted, in the mind of the public and of many health care leaders, diagnostic variation is becoming increasingly equated with error. He further states that like any other medical problem, diagnostic disagreement should be approached as much as possible using a scientific framework.38 We might ask, ‘‘Will that be enough to satisfy public concern?’’ Scientific studies require time and resources. Time in the busy surgical pathology laboratory is generally in short supply, and grant funding or practice revenue to study error reduction in any part of medicine has so far been scant.

Currently, pathology appears to be operating at about a 2.0% error rate. This may be a charitable figure. If pathology reached a level of being 99.9% error free, per the study

by Leape39 of errors in medicine, this would still mean in business terms 2 unsafe plane landings at O’Hare airport per day, 16 000 pieces of lost mail every hour, and 32 000 bank checks deducted from the wrong account every hour.

When we are on that plane, did not receive the bill in the mail, or had to call our bank, we are not happy.

How should we then address the question of error in pathology? This author suggests continuing well-constructed studies to identify errors and particularly their source. The disconnect between experts’ reporting of Gleason score on prostate needle biopsy and the perception of the general pathology community is a good example of identifying a problem area and one that can be remedied by education via on-line learning. Standardization of grading and reporting of biopsies, particularly in common problem areas, is another example. By using standardized reporting terminology and diagnostic formatting of reports within a given pathology group or across many groups, clinicians cannot identify either the specific pathologist or group who reviewed the material. Standardization and redundancy are 2 methods that have worked for the airline industry, and they have potential merit for application in pathology. Finally, physicians should communicate with patients as patient advocates. Educate them to understand the science, that is, that medicine is fundamentally the assessment of risk. Perhaps there is a need for pathology bloggers. Unlike the media, pathology is in a unique position to see the big picture, but to present it in valid scientific terms. Remember that medical news focuses on the bad and the sensational. This generates public concern. Public concern often translates into political concern. Political concern translates into legislation. Legislation leads to regulation and testing. All of this overtook the cytopathology community. Ask yourself if you would like to be tested each year on your proficiency in surgical pathology.

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35. Renshaw AA, Schultz D, Cote K, Loffredo M, Ziemba DE, D’Amico AV. Accurate Gleason grading of prostatic adenocarcinoma in prostate needle biopsies by general pathologists. Arch Pathol Lab Med. 2003;127:1007–1008.

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