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Original article
Improved quality of patient care through routine second review of histopathology specimens prior to multidisciplinary meetings
  1. Chantal C H J Kuijpers1,2,3,
  2. Gerard Burger1,
  3. Shaimaa Al-Janabi1,
  4. Stefan M Willems2,
  5. Paul J van Diest2,
  6. Mehdi Jiwa1,2
  1. 1Symbiant Pathology Expert Centre, Alkmaar, The Netherlands
  2. 2Department of Pathology, University Medical Centre Utrecht, Utrecht, The Netherlands
  3. 3PALGA, Houten, The Netherlands
  1. Correspondence to Dr Mehdi Jiwa, Department of Pathology, Alkmaar Medical Centre, Symbiant Pathology Expert Centre, P.O. Box 501, Alkmaar 1815 JD, The Netherlands; m.jiwa{at}symbiant.nl

Abstract

Aim Double reading may be a valuable tool for improving quality of patient care by identifying diagnostic errors before final sign-out, but standard double reading would significantly increase costs of pathology. We assessed the added value of intradepartmental routine double reading of histopathology specimens prior to multidisciplinary meetings.

Methods Diagnoses, treatment plans and prognoses of patients are often discussed at multidisciplinary meetings. As part of the daily routine, all pathology specimens to be discussed at upcoming multidisciplinary meetings undergo prior intradepartmental double reading. We identified all histopathology specimens from 2013 that underwent such double reading and determined major and minor discordance rates based on clinical relevance between the initial and consensus sign-out diagnoses.

Results We included 6796 histopathology specimens that underwent double reading, representing approximately 8% of all histopathology cases at our institution in 2013. Double reading diagnoses were concordant in 6566 specimens (96.6%). Major and minor discordances were observed in 60 (0.9%) and 170 (2.5%) specimens, respectively. Urology specimens had significantly more discordances than other tissues of origin, Gleason grading of prostate cancer biopsies being the most frequent diagnostic problem. Furthermore, premalignant and malignant cases showed significantly higher discordance rates than the rest. The vast majority (90%) of discordances represented changes within the same diagnostic category (eg, malignant to malignant).

Conclusions Routine double reading of histopathology specimens prior to multidisciplinary meetings prevents diagnostic errors. It resulted in about 1% discordant diagnoses of potential clinical significance, indicating that second review is worthwhile in terms of patient safety and quality of patient care.

  • HISTOPATHOLOGY
  • QUALITY ASSURANCE
  • DIAGNOSTICS
  • SAFETY

https://doi.org/10.1136/jclinpath-2015-203488

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    Introduction

    There is a growing awareness that pathology diagnosis is not infallible and that diagnostic errors may lead to undertreatment or overtreatment and thereby compromise patient safety. Double reading —that is, second assessment of pathology cases—is a potentially valuable tool for reducing diagnostic errors and thereby improving the quality of patient care. It may reveal inaccurate diagnoses that otherwise might have led to improper patient management. In response to the Institute of Medicine's report ‘To err is human; building a safer health system’ in 1999,1 the American Society for Clinical Pathology (ASCP) recognised double reading of pathology cases as a key aspect in the assurance of patient safety.2 The ASCP recommends considering double reading in highly critical or significant cases, problem-prone cases and cases suggested for review by clinicians.2

    Numerous studies have assessed the value of double reading in diagnostic surgical pathology and reported major diagnostic disagreement rates of 0.1–28%, mainly depending on the organ system studied and the definition of disagreement.3–29 Intradepartmental second review resulted in 0.1–2.8% disagreements with potential clinical significance.3–6 ,15 ,18 ,19

    At our institution, pathology specimens of patients who will be discussed at the upcoming multidisciplinary meetings undergo prior intradepartmental double reading, most of the time by an expert pathologist. In this study we retrospectively assessed the added value of this double reading strategy in improving diagnostic accuracy in a large 1-year cohort of reviewed histopathology cases by assessing (degree of) concordance between the initial and the consensus sign-out diagnoses.

    Materials and methods

    Routine double reading prior to multidisciplinary meetings

    Symbiant provides pathology services for six public healthcare non-academic teaching hospitals in the province of North Holland. In these hospitals, diagnoses, treatment plans and prognoses of patients are discussed at multidisciplinary meetings. Cases to be discussed at these multidisciplinary meetings vary from all cases in the specific medical discipline of the multidisciplinary meeting to only exceptional cases which differ from routine guidelines.

    At Symbiant's three pathology laboratories (Alkmaar Medical Centre, Westfriesgasthuis Hoorn and Zaandam Medical Centre), all pathology specimens to be discussed at the upcoming multidisciplinary meetings routinely undergo prior intradepartmental double reading at preparation for each multidisciplinary meeting, based on lists from the responsible clinician. The second review is performed in a non-blinded fashion by the pathologist who will attend the meeting, most of the time an expert pathologist in the field of that multidisciplinary meeting. Cases reported by a resident are routinely checked by a pathologist before sign-out, which is not considered as double reading.

    The pathologists register the results of the second review (ie, concordant or discordant) in a ‘hidden’ section of the pathology reporting system, which is not visible to clinicians. Discordant diagnoses are fed back to and discussed with the pathologist who made the initial pathology report. Consensus diagnoses are then formulated, achieved either by unanimity or by majority, following consensus joint review by the first and second pathologists or after consulting other colleague pathologists. The final report only contains the consensus sign-out diagnosis. Previous versions of the report are stored in a separate section of the pathology reporting system, unavailable to clinicians as well, highlighting the changes made.

    Data extraction

    All pathology reports of histopathology specimens from 2013 that underwent routine double reading prior to a multidisciplinary meeting were identified by automatic search for a specific code (ie, internal revision). The initial diagnoses and the consensus sign-out diagnoses were extracted from the ‘hidden’ previous version of the report and the final report, respectively. Specimens for which we were not able to determine the diagnostic concordance of the double reading due to the unavailability of the original pathology reports were excluded from analysis.

    The study cases were sorted according to their tissue of origin and diagnostic categories. Diagnoses were categorised as no abnormalities, benign (including reactive, inflammation, benign tumour and other benign abnormalities such as hemochromatosis and amyloidosis), uncertain malignant potential, premalignant, suspicious for malignancy, malignant (including primary and metastatic malignancy) and no diagnosis.

    Assessment of concordance between initial and second review diagnoses

    Initial and consensus sign-out diagnoses were retrospectively compared to determine (the degree of) concordance after double reading. A discordant double reading was categorised as minor discordant or major discordant based on clinical significance. Minor discordance was defined as a change in diagnosis that would not alter patient management or prognosis, whereas major discordance was defined as a changed diagnosis with a potential effect on patient management or prognosis.

    Statistical analysis

    Statistical analysis was performed using SPSS Statistics for Windows V.20.0 (IBM, Armonk, New York, USA). The percentages of concordance, major discordance and minor discordance between initial and consensus sign-out diagnoses with their 95% CIs were calculated. The χ2 test statistic was used to compare the percentages of overall, major and minor discordance between each individual tissue of origin and the rest, and between each individual diagnostic category and the rest. Furthermore, the categories of initial diagnosis and consensus sign-out diagnosis were compared using the unweighted Cohen' κ coefficient. A κ value of 0.00–0.20 indicates slight agreement, 0.21–0.40 fair agreement, 0.41–0.60 moderate agreement, 0.61–0.80 substantial agreement and 0.81–1 (almost) perfect agreement.30 ,31 p Values <0.05 were considered statistically significant.

    Results

    Figure 1 illustrates the flowchart of the histopathology specimens originating from 2013 that underwent double reading. We included 6796 unique histopathology specimens from 4388 patients, representing approximately 8% of all histopathology cases from 2013. The double reading of these specimens was performed by 22 different pathologists in total. The tissue of origin and the initial diagnoses of the included histopathology specimens are summarised in table 1. Most (56.7%) of the cases that underwent second review originated from the breast and the gastrointestinal tract. With regard to initial diagnosis, the majority (59.5%) of the cases that underwent second review were malignant.

    View this table:
    Table 1

    Overview of the 6796 included histopathology specimens undergoing routine double reading

    Figure 1
    Figure 1

    Flowchart of specimens included in the study.

    Consensus sign-out diagnoses were concordant with initial diagnoses in 6566 specimens (96.6%; 95% CI 0.962% to 0.970%) and discordant in 230 specimens (3.4%), with minor and major discordance in 170 specimens (2.5%; 95% CI 0.021% to 0.029%) and 60 specimens (0.9%; 95% CI 0.007% to 0.011%), respectively.

    Table 2 summarises the percentages of major, minor and overall discordance observed per tissue of origin. The overall discordance rates of bone and joint, lymph node and breast specimens were significantly lower, which was mainly explained by a lower frequency of minor discordances. Significantly fewer major discordances were encountered with specimens from the gastrointestinal tract and there were significantly more discordances with urology specimens than with the rest, Gleason grading of prostate cancer biopsies being the most frequent diagnostic problem. Of the 402 prostate specimens, 16 (4.0%) major discordances were encountered. Without second review of these prostate cancer biopsies, the patients would probably have been undertreated (n=7) or overtreated (n=7) because of underestimation or overestimation of the Gleason grade, respectively. Treatment of the other two patients would probably have been suboptimal as well (a change from Gleason grade not assessable into Gleason grade 7 and a change from tumour only present in the left-sided biopsies into right-sided biopsies containing tumour as well).

    View this table:
    Table 2

    Percentages of discordance observed after double reading per tissue of origin

    Table 3 summarises the percentages of discordance observed per initial diagnostic category. Second review of specimens with no abnormalities and with a benign diagnosis resulted in significantly lower discordance rates than the other diagnostic categories. For the benign cases, both major and minor discordance rates were significantly lower. Significantly more overall discordances were encountered with malignant and premalignant cases than with the rest. For the malignant cases, this was mainly explained by a higher proportion of minor discordances, whereas premalignant cases had a significantly higher proportion of major discordances than the rest.

    View this table:
    Table 3

    Percentages of discordance observed after double reading per initial diagnostic category

    Table 4 presents the correlation between diagnostic categories of initial and second review diagnoses. The diagnostic category remained the same for 6773 specimens (99.7%; κ=0.99, p<0.0001). A change in diagnostic category was observed for 23 specimens (0.3%), which represents 10.0% of overall discordances. The other discordances represented a change within the same diagnostic category. These included changes in histological subtype, margin status, grade, TNM stage, tumour diameter, tumour percentage, the number of malignant biopsies, the number of (metastatic) lymph nodes without changing TNM stage, the number of mitoses without changing TNM stage or HER-2 oncogene status. Other discordances within the same diagnostic category were missed unsolicited findings (eg, an additional in situ lesion in a case of carcinoma), the need for additional material, typographical errors or different terminology used, a change in clinical information, an incomplete pathology report and other minor differences in interpretation without clinical relevance. All malignant cases retained the diagnosis of malignancy after second review. In these cases, only changes within the same diagnostic category (ie, malignant) were observed (eg, changes in grade or margin status).

    View this table:
    Table 4

    Correlation between diagnostic categories of initial diagnoses and consensus sign-out diagnoses

    Discussion

    This study assessed the added value of intradepartmental routine double reading of histopathology specimens prior to discussion at multidisciplinary meetings. Initial and second review diagnoses were concordant in 96.6% of cases. Major discordances with a potential clinical significance were observed in 60 cases (0.9%). The vast majority (90%) of discordances were changes within the same diagnostic category rather than changes into another diagnostic category. Our observed major discordance rate of 0.9% falls within the range of discordance rates (0.1–2.8%) with potential clinical significance described in the literature concerning intradepartmental second review of surgical pathology specimens.3–6 ,15 ,18 ,19

    Urology specimens had an overall discordance rate of 9.6% and a major discordance rate of 2.8%, both significantly higher than the other tissues of origin. Weydert et al18 also found most major discordances in the urological tract. Contrary to our study, Lind et al6 described no major discordances in genitourinary biopsies, while the highest rates of major discordance were observed in pulmonary and head and neck specimens. The discordances observed in urology specimens particularly concerned prostate biopsies, especially a change in Gleason grade. It is well known that the interobserver agreement of Gleason grading is unsatisfactory,32 ,33 although accurate grading may be essential for optimal treatment selection. Several studies comparing prostate biopsy first and second review diagnoses found a change in Gleason score in approximately 40%.10 ,17 Furthermore, Wurzer et al10 showed that, in 5% of patients, second review resulted in treatment modifications, either due to misdiagnosis of prostate cancer, change in Gleason grade or missed presence of perineural invasion.

    In the present study, significantly higher discordance rates were observed in premalignant and malignant cases compared with the other diagnostic categories. Still, five cases (0.4%) that were initially diagnosed as benign had a discrepancy after double reading with potential clinical significance, of which three originated from the skin. Romanoff et al34 studied second reviews of breast biopsies and found that benign biopsies were more likely to result in a discrepancy than malignant cases. Troxel35 demonstrated that most pathology malpractice claims resulted from false-negative diagnoses, especially missed melanomas. These results indicate that, ideally, a selection of problem-prone benign cases should undergo double reading as well. Benign skin and breast lesions may therefore be interesting for second review. Most of the discordances concerned changes within the same diagnostic category (eg, benign to benign), rather than changes into another diagnostic category (eg, benign to malignant). On the contrary, in the study by Weydert et al18 the majority of the reported major discordances were due to changes into another diagnostic category.

    The double reading strategy described here was performed in addition to usual upfront consultation that might have already been performed at the time of second review, but still resulted in a substantial number of changed diagnoses: 60 major discordances per year where double reading possibly led to a change in patient management. This emphasises the need for a systematic double reading strategy. Very recently published recommendations of the College of American Pathologists (CAP) and the Association of Directors of Anatomic and Surgical Pathology (ADASP) for the review of pathology cases also emphasise this.36 They recommend that anatomic pathologists should develop procedures for the review of selected pathology cases, perform case reviews in a timely manner (prior to definitive treatment), document case review procedures that are relevant to their practice setting, continuously monitor and document the results of case reviews and take steps to improve agreement if pathology case reviews show poor agreement within a defined case type.36 We fully agree with these recommendations, which we deem to be appropriate, feasible and necessary for good pathology practice, depending on the practice setting.

    Although the CAP/ADASP recommend that double reading should be performed prospectively (ie, before sign-out), our retrospective double reading strategy is also considered timely according to the CAP/ADASP guidelines as it is still performed prior to definitive treatment. Although second review was performed after sign-out, it is clear to the clinicians that the definitive pathology diagnosis is rendered at the multidisciplinary meeting. Prospective second review of the same specimens would probably have been less rework in corrections without changing the results of second review. However, routine second review before sign-out increases turnaround times, which may be a particular problem in cases where small turnaround times are warranted.

    There is no single best double reading strategy as this varies with practice setting. Double reading strategies can either comprise reviewing every (histo)pathology case, a fixed percentage of randomly selected cases or known problem-prone tissues of origin. The literature is not consistent as to which specimen types are most problem-prone,36 and this may also vary between laboratories. Therefore, as part of quality control, pathology laboratories might want to determine annually for their specific case mix which specimens/tracts/organs are problem-prone and focus their double reading strategy on these areas. The cases included in this study were, on average, probably somewhat more difficult than the routine of the department which contains, for example, a high percentage of relatively easy skin and gastrointestinal biopsies, of which only a small proportion are reviewed prior to and discussed at a multidisciplinary meeting.

    A weakness of this study is that we did not assess on an individual basis whether a discrepancy would lead to an actual change in patient management. The expected effect on prognosis and patient management was determined by specialised pathologists according to guidelines and experience. Furthermore, although we cannot be totally sure, we considered the consensus sign-out diagnosis, involving a specialised pathologist, to be the correct diagnosis.

    We consider the increase in workload and costs of double reading and associated administrative actions worth the effort, given the large added value in terms of minimising diagnostic errors to improve quality of patient care and to prevent claims due to diagnostic error. The additional time spent by pathologists on double reading should be incorporated into the cost price of the pathology service.

    In conclusion, routine double reading of histopathology specimens prior to multidisciplinary meetings resulted in about 1% discordant diagnoses of potential clinical significance, indicating that second review is worthwhile in terms of patient safety and quality of patient care. An adequate quality improvement programme requires some routine double reading, which should be financially covered, independent of the funding model.

    Take home messages

    • Double reading of pathology specimens is a potentially valuable tool for reducing diagnostic errors and thereby improving the quality of patient care.

    • Routine double reading of histopathology specimens prior to multidisciplinary meetings resulted in about 1% discordant diagnoses of potential clinical significance, indicating that second review is worthwhile in terms of patient safety and quality of patient care.

    • Urology specimens had significantly more discordances than the other tissues of origin, Gleason grading of prostate cancer biopsies being the most frequent diagnostic problem.

    • Although premalignant and malignant cases showed the highest discordance rates, five benign cases also had a major discrepancy after double reading. Therefore benign cases may also be interesting for second review.

    Acknowledgments

    The authors would like to thank all the involved pathologists of Symbiant.

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    Footnotes

    • Handling editor Cheok Soon Lee

    • Contributors CCHJK and MJ designed the study, GB identified all pathology reports of specimens that underwent double reading, GB determined the (degree of) concordance together with specific expert pathologists of Symbiant, CCHJK and SA-J analysed the data, CCHJK wrote the manuscript, all authors read and agreed with the article.

    • Competing interests None declared.

    • Ethics approval This was a quality improvement study approved by the head of the department. No external ethical approval was necessary as we consider our study to comply with exemption 4 of the Federal Policy for the Protection of Human Subjects.37

    • Provenance and peer review Not commissioned; externally peer reviewed.