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Comparison of Clinical Diagnoses and Autopsy Findings: Six-Year Retrospective Study.

Hospital autopsy rates in the United States declined from 30% to 40% in the 1960s (1) to 8% in the early 2000s. (2) Multiple factors, such as the elimination of the hospital autopsy rate requirement in 1972, lack of reimbursement, cultural and religious objections by families, and increasing workload for house staff, account for the decrease. (3) Even as sophisticated medical technologic tools have been developed and made available, the role of the autopsy for confirming clinical diagnoses and identifying unsuspected findings should be reevaluated regularly. Herein, we report our findings of the importance of the autopsy by comparing the clinical diagnosis with the anatomic findings in a single large academic institution between the years of 2009 and 2014.

MATERIALS AND METHODS

Clinical information of all adult (18 years or older) autopsy cases performed in Jackson Memorial Hospital (Miami, Florida) for 6 years (from January 2009 to December 2014) was retrospectively evaluated. Only cases with a stay longer than 24 hours in Jackson Memorial Hospital were included in the study in order to ensure enough time for initial clinical evaluation and management. Exclusion criteria were: (1) a hospital stay of less than 24 hours, (2) restrictions to single-organ or body cavity dissections, and (3) cases referred from other facilities. Cases from the University of Miami Hospital (Miami, Florida), which shares attending physicians and residents in the adjacent campus and whose full medical records were available, were considered in-house cases.

All cases had consent for autopsy from the legal next of kin, and each autopsy was performed by pathology residents who observed restrictions, if there were any. Attending pathologists directly supervised each case. For each eligible autopsy the autopsy report, including clinical history, was reviewed by 2 pathologists (H.M. and C.M.). Medical records were reviewed if the clinical information provided in the autopsy report was unclear or inadequate. Each case was classified using the Goldman Classification (Table 1).4 When a case could be classified with more than one discrepancy, the higher class (smaller number) was regarded as the final classification. The pathologists reviewed the cases independently, compared their assessments, and came to consensus by discussion if there was discordance.

The study design was reviewed by the Institutional Review Board of the University of Miami and approved to be conducted as nonhuman research.

RESULTS

Of 923 autopsies performed in Jackson Memorial Hospital for the 6 years (2009-2014), 512 cases (55.5%) were performed on adults (age >18 years). A total of 334 of 512 cases (65.2%) were subject to review after excluding those with a short (<1 day) hospital stay, restriction to a single-organ or body cavity dissection, and those referred from other facilities (Table 2). The demographics of the patients included are presented in Table 3.

A total of 33 of 334 cases (9.9%) were identified as a class I discrepancy, where the autopsy revealed a discrepant diagnosis with a potential impact on survival or treatment (Table 4). Various critical findings, such as untreated infection (15 of 33 cases; 45.5%), pulmonary embolism (8 of 33 cases; 24.2%), and undiagnosed malignancy (6 of 33 cases; 18.2%) were identified in cases of this class (Table 5). For the cases with class I discrepancies, the clinical history or impression and critical laboratory or imaging results are listed in Table 6. Major significant findings that had not been clinically detected, whether they might or might not have clinical impact, were found in a total of 65 of 334 cases (class I and II; 19.5%).

DISCUSSION

This study is a retrospective review of the adult autopsy reports for recent years in the third largest public hospital (1550 beds) in the United States. It excluded cases from outside institutions, patients with short hospital stays, and those in which the autopsy was restricted to a single organ or body cavity, in order to optimize the clinical and pathologic correlation. Even though the exclusion made the size of the study smaller, the entire set of included cases was comprehensively reviewed, unlike in some previous studies which only reviewed randomly sampled cases. (5)

There was a limitation to calculate the exact autopsy rate because: (1) some cases were declared to be under the jurisdiction of the medical examiner, and therefore dropped from the initial data set, and (2) Jackson Memorial Hospital has many branches and affiliated hospitals from which autopsies are requested, and the total number of deaths in each hospital was not available.

Despite intensive modern clinical investigations, autopsies have continued to reveal major antemortem diagnostic errors in as many as 30% of cases. (6-8) Follow-up or meta-analysis studies show that the rate of clinically significant discrepancy is decreasing over decades; however, 4% to 7% of cases still have class I discrepancies. (1,5) This study shows a comparable result of 9.9% of clinically significant findings to the previous studies.

Undiagnosed infections, especially pneumonia, and pulmonary embolism were the 2 most common significant unexpected findings. These are common complications of hospitalization and subsequent immobilization. The character of the study, which excluded the short hospital stay, may make the frequency of those complications more notable by a possible exclusion of sudden cardiovascular accidents, which might have a significant portion in autopsies but have a short time period between the initial clinical presentation and the patient's demise. Because early suspicion and detection may make for a significantly better prognosis in those potentially fatal complications, vigilant management for preventing these conditions is suggested.

Beyond the direct clinical or administrative advantages, autopsies have other virtues, such as educational and epidemiologic values. (9) The autopsy should continue to be the gold standard for quality control in clinical management, including radiologic evaluation, (10-15) in spite of declining requests. (16) The most crucial factors influencing attitudes toward the autopsy have been shown to be the clinician's level of experience with autopsy in training and practice. Therefore, the importance of the autopsy should be emphasized in medical education and postgraduate training so the number of significant diagnostic discrepancies can be reduced and patient care can be optimized.

Please Note: Illustration(s) are not available due to copyright restrictions.

References

(1.) Shojania KG, Burton EC, McDonald KM, Goldman L. Changes in rates of autopsy-detected diagnostic errors over time: a systematic review. JAMA. 2003; 289(21):2849-2856.

(2.) National Center for Health Statistics. Autopsy Patterns in 2003: Data on Mortality. Hyattsville, MD: US Dept of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics; 2007.

(3.) Scordi-Bello IA, Kalb TH, Lento PA. Clinical setting and extent of premortem evaluation do not predict autopsy discrepancy rates. Mod Pathol. 2010; 23(9):1225-1230.

(4.) Goldman L, Sayson R, Robbins S, Cohn LH, Bettmann M, Weisberg M. The value of the autopsy in three medical eras. N Engl J Med. 1983; 308(17):1000-1005.

(5.) Schwanda-Burger S, Moch H, Muntwyler J, Salomon F. Diagnostic errors in the new millennium: a follow-up autopsy study. Mod Pathol. 2012; 25(6):777-783.

(6.) Spiliopoulou C, Papadodima S, Kotakidis N, Koutselinis A. Clinical diagnoses and autopsy findings: a retrospective analysis of 252 cases in Greece. Arch Pathol Lab Med. 2005; 129(2):210-214.

(7.) Tavora F, Crowder CD, Sun CC, Burke AP. Discrepancies between clinical and autopsy diagnoses: a comparison of university, community, and private autopsy practices. Am J Clin Pathol. 2008; 129(1):102-109.

(8.) Gonzalez-Franco MV, Ponce-Camacho MA, Barboza-Quintana O, Ancer-Rodriguez J, Cecenas-Falcon LA. Discrepancies between clinical and autopsy diagnosis: a study of 331 autopsies performed over a 7 years period. Medicina Universitaria. 2012; 14(54):16-22.

(9.) Burton JL, Underwood J. Clinical, educational, and epidemiological value of autopsy. Lancet. 2007; 369(9571):1471-1480.

(10.) Bauer TM, Potratz D, Goller T, Wagner A, Schafer R. Quality control by autopsy: how often do the postmortem examination findings correct the clinical diagnosis [in German]? Dtsch Med Wochenschr. 1991; 116(21):801-807.

(11.) Grundmann E. Autopsy as clinical quality control: a study of 15, 143 autopsy cases. In Vivo. 1994; 8(5):945-952.

(12.) Hasan M, Woodhouse K. Autopsy: its role in clinicalquality controlin the elderly in the 1990s. Arch Gerontol Geriatr. 1995; 21(2):199-203.

(13.) Murken DR, Ding M, Branstetter BF 4th, Nichols L. Autopsy as a quality control measure for radiology, and vice versa. AJRAm J Roentgenol. 2012; 199(2): 394-401.

(14.) Sebok J, Magyar E, Csanadi C, Csaky A, Schonfeld T. The importance of the autopsy in quality control of medicine (possibilities in the Hungarian conditions). Orv Hetil. 2005; 146(33):1711-1720.

(15.) Solheim K. Quality control in the last round: autopsy is still necessary [in Norwegian]! Tidsskr Nor Laegeforen. 1993; 113(20):2553.

(16.) Hooper JE, Geller SA. Relevance of the autopsy as a medical tool: a large database of physician attitudes. Arch Pathol Lab Med. 2007; 131(2):268-274.

Hyejong Song Marshall, MD; Clara Milikowski, MD

Accepted for publication December 29, 2016.

Published as an Early Online Release June 28, 2017.

From the Department of Pathology and Laboratory Medicine, Jackson Memorial Hospital/University of Miami, Miami, Florida.

The authors have no relevant financial interest in the products or companies described in this article.

The data and abstract were presented at the annual meeting of the United States and Canadian Academy of Pathology (USCAP); March 14, 2016; Seattle, Washington.

Reprints: Clara Milikowski, MD, Pathology and Laboratory Medicine, Jackson Memorial Hospital/University of Miami, 1611 NW 12th Ave, Holtz Children's Hospital, 2nd Floor, Suite 2042, Miami, FL 33136 (email: CMilikowski@med.miami.edu).
Table 1. Criteria of Goldman Classification

        Type of
Class   Discrepancy   Definition              Example: Death Due
                                              to:

I       Major         Directly related to     Unsuspected
                      death; if               myocardial
                      recognized, may have    infarction
                      altered treatment or    presenting with
                      survival                chest pain

II      Major         Directly related to     Unsuspected
                      death; if recognized,   myocardial
                      would not have          infarction
                      altered treatment or    presenting with
                      survival                cardiac arrest

III     Minor         Incidental autopsy      Known myocardial
                      finding not directly    infarction with
                      related to death but    unsuspected left
                      related to terminal     ventricular mural
                      disease process         thrombus

IV      Minor         Incidental autopsy      Known myocardial
                      finding unrelated to    infarction with
                      cause of death          unsuspected lung
                                              cancer

V       No error      Clinical and autopsy
                      diagnoses in
                      complete agreement

Table 2. Numbers of Cases Included and Excluded by Year

Year                                       2009   2010   2011   2012

Total number of autopsies (A)              204    151    140    154
Cases of age older than 18 y (B)           107     66     76    105
Outside case (C)                             6      2      4      6
Short (<1 d) stay (D)                       21     14      8     23
Single organ or single cavity only (E)       6      4      8      9
Cases subject to review (B-[C + D + E])     74     46     56     67

Year                                       2013   2014   Total

Total number of autopsies (A)              137    137     923
Cases of age older than 18 y (B)            74     84     512
Outside case (C)                             6      5      29
Short (<1 d) stay (D)                       13     17      96
Single organ or single cavity only (E)      13     13      53
Cases subject to review (B-[C + D + E])     42     49     334

Table 3. Patient Demographics

Item        No. (%)

Sex
  Male     189 (56.6)
  Female   145 (43.4)
Total      334 (100)
Age, y
  18-30     38 (11.4)
  31-40     22 (6.6)
  41-50     43 (12.9)
  51-60     89 (26.6)
  61-70     85 (25.4)
  71-80     42 (12.6)
  >80       15 (4.5)
Total      334 (100)

Table 4. Result of Case Classification

Class   No. (%) of Cases

I        33 (9.9)
II       32 (9.6)
III      12 (3.6)
IV      110 (32.9)
V       147 (44.0)
        334 (100)

Table 5. Findings With Potential Impact on Survival
or Treatment (Class I Discrepancy)

Item and Findings                              No. (%)

Infection                                     15 (45.5)
  Fungal pneumonia (1 case with coexisting        6
    fungal myocarditis)
  Viral pneumonia                                 2
  Bacterial pneumonia                             2
  Miliary tuberculosis and bacterial              1
    meningitis
  Meningitis of unknown etiology                  1
  Toxoplasmosis involving lung, liver, and        1
    brain
  Candidemia confirmed by postmortem              1
   blood culture
  Renal abscess                                   1
Pulmonary embolism                            8 (24.2)
Malignancy                                    6 (18.2)
  Lymphoma involving multiple organs              3
    Diffuse large B-cell lymphoma
    Follicular lymphoma
    Peripheral T-cell lymphoma
  Pulmonary carcinoma                             2
    Small cell carcinoma
    Squamous cell carcinoma
  Gastric adenocarcinoma                          1
Cardiovascular                                 3 (9.1)
  Retroperitoneal and/or intraabdominal           2
    hemorrhage
  Cartilaginous emboli                            1
Immunologic                                    1 (3.0)
  Anaphylactic laryngeal edema                    1
Total                                         33 (100)

Table 6. Clinical History or Impression and Critical Labs or
Imaging Compared With Class I Autopsy Findings

Serial   Age, y/Sex   Clinical History or Impression

1        34/M         History of stroke, shortness of
                      breath, flulike symptoms,
                      possible pneumonia

2        81/M         DM, valvular heart disease, fever
                      and chills after procedure for
                      benign prostatic hyperplasia

3        68/F         DM, HTN, ischemic
                      cardiomyopathy

4        83/F         Myasthenia gravis, pneumonia

5        64/F         COPD aggravation

6        56/M         DM, HTN, nausea, vomiting,
                      chest pain

7        68/M         Pneumonia

8        48/F         Mixed connective tissue disease,
                      sepsis by multiple organisms

9        65/F         Leukemia, s/p bone marrow
                      transplant

10       65/F         s/p liver transplant, transfusion of
                      red blood cells to correct anemia

11       55/M         Admitted for schizophrenia,
                      COPD

12       58/M         Adrenal mass, steroid therapy for
                      numbness

13       54/M         s/p kidney transplant, hematuria
                      and abdominal pain, chest pain

14       43/F         HIV, HTN, hypertensive crisis

15       77/M         Dementia, HTN, normal pressure
                      hydrocephalus, hematemesis

16       59/M         POEMS syndrome, vomiting

17       39/M         Neck pain, complicated hospital
                      course including pulmonary
                      embolism

18       57/M         DM, s/p kidney and pancreas
                      transplant, nausea and
                      abdominal pain

19       69/M         Lymphoma, s/p chemotherapy,
                      rash, fever

20       23/F         36-wk pregnancy, pulmonary
                      infiltrates, emergency cesarean
                      delivery

21       58/M         Inguinal hernia, persistent HTN
                      after surgery

22       30/F         Anti-NMDA receptor autoimmune/
                      paraneoplastic encephalitis

23       54/M         HTN, DM, s/p kidney transplant,
                      pulmonary edema, acute renal failure

24       58/F         DM, HTN, weight loss,
                      lymphadenopathy, shortness of
                      breath

25       50/F         Bronchiectasis, cirrhosis due to
                      probable autoimmune hepatitis,
                      hemoptysis

26       41/M         HTN, sickle cell trait, after elective
                      lumbar disk surgery, abdominal
                      pain and respiratory failure,
                      renal injury, disseminated
                      intravascular coagulation,
                      possible septicemia

27       62/F         HTN, autoimmune hepatitis
                      overlap with primary biliary
                      cirrhosis, varices, hepatorenal
                      syndrome, acute respiratory
                      distress syndrome

28       74/F         Cirrhosis, pleural effusion,
                      aspiration pneumonia

29       54/F         Asthma, cough, chest pain,
                      antibiotic treatment, diarrhea,
                      biopsy was planned but not
                      done

30       20/M         Cerebral palsy, hydrocephalus s/p
                      shunt, hip dislocation s/p
                      replacement. Septic shock.
                      Treated with antibiotics

31       42/M         HIV, DM, congestive heart failure,
                      atrial fibrillation

32       58/M         Gout, asthma, HTN, atrial
                      fibrillation, extremity weakness,
                      and altered speech

33       76/F         Bladder and upper urinary tract
                      cancer, DM, coronary artery
                      disease, sudden collapse in
                      hospital stay for urinary tract
                      infection

Serial   Critical Lab or Imaging

1        Diffuse nodularity on chest
         radiograph, MSSA in blood

2        Blood and urine culture negative

3        Atrial fibrillation

4        Pneumonia and pulmonary
         edema, Proteus bacteremia

5        Hilar lymphadenopathy on
         imaging, BAL with Candida

6        Hepatitis C virus positive with
         elevated liver enzymes, cardiac
         enzyme negative

7        Blood culture negative, pleural
         effusion, consolidation of lung

8        Rhabdomyolysis, CMV, Klebsiella,
         Acinetobacter, Enterococcus

9        Elevated liver enzymes, negative
         blood culture and BAL

10       Bibasilar opacity and pleural
         effusion on chest radiograph

11

12       Adrenal mass, pleural effusion on
         imaging, hypercalcemia

13       Nonsignificant electrocardiogram
         and troponin

14       Pulmonary edema and enlarged
         cardiac silhouette, positive for
         cocaine

15

16       Hepatomegaly, spontaneous
         bacterial peritonitis

17       Edema of spinal cord

18       Leukocytosis

19       Pulmonary interstitial edema on
         chest radiography, gram-
         negative rods in bone marrow
         culture

20       Pulmonary embolism workup with
         negative results

21       Lung consolidation with mild
         pleural effusion

22       Infection workup with negative
         results

23       Leukopenia

24       Pulmonary embolism workup with
         negative result

25       Soft tissue mass encasing the
         celiac vessels and pericardium,
         mild elevation of aspergillosis
         glucomannan level

26       Decreasing hemoglobin and
         hematocrit

27       Chronic cholestatic hepatitis on
         liver biopsy, Klebsiella
         bacteremia

28       MSSA bacteremia, blood culture
         positive for Klebsiella, aspiration
         pneumonia on chest radiograph

29       Lung opacity concerning for
         infection, multiple enlarged
         lymph nodes

30       Hypernatremia, coagulopathy

31       Hyponatremia, marked and
         diffuse cerebral edema, MSSA
         bacteremia, pulmonary opacity;
         consolidation versus atelectasis

32       Brain CT with no intracranial
         hemorrhage

33       Mild interstitial pulmonary edema
         on chest radiograph

Serial   Significant Autopsy Findings

1        Pulmonary embolism

2        Pulmonary embolism

3        Pulmonary embolism

4        CMV pneumonia and colitis,
         not bacterial

5        Small cell carcinoma of lung
         with metastasis to lymph
         nodes and bone

6        Acute retroperitoneal
         hemorrhage extending into
         abdominal cavity

7        HSV pneumonia, not bacterial
         or fungal

8        Fungal pneumonia, not just
         viral and bacterial

9        Toxoplasmosis involving lung,
         liver, and brain

10       Laryngeal edema

11       Squamous cell carcinoma of
         lung

12       Diffuse large B-cell
         lymphoma, meningeal
         malignant lymphomatosis

13       Pulmonary embolism

14       Chronic meningitis of
         undetermined etiology

15       Bacterial pneumonia

16       Follicular lymphoma

17       Cartilaginous emboli to cervical
         spinal cord, recent hematoma
         of thalamus

18       Intra-abdominal and
         retroperitoneal hemorrhage

19       Fungal pneumonia

20       Pulmonary embolism

21       Pulmonary embolism

22       Pulmonary embolism

23       Abscesses of transplanted
         kidney

24       Poorly differentiated
         adenocarcinoma of stomach
         with metastasis to vertebral
         bone marrow
25       Fungal pneumonia and
         myocarditis

26       Fungal pneumonia

27       Fungal pneumonia

28       Fungal pneumonia

29       Peripheral T-cell lymphoma

30       Candidemia confirmed by
         postmortem blood culture

31       Miliary tuberculosis. Acute
         meningitis suggestive of
         bacterial etiology

32       Pulmonary embolism

33       Bacterial pneumonia

Abbreviations: BAL, bronchoalveolar lavage; CMV, cytomegalovirus;
COPD, chronic obstructive pulmonary disease; CT, computed
tomography; DM, diabetes mellitus; HIV, human immunodeficiency
virus; HSV, herpes simplex virus; HTN, hypertension; MSSA,
methicillin/sensitive Staphylococcus aureus; NMDA,
N/methyl/D/aspartate; POEMS, polyneuropathy, organomegaly,
endocrinopathy, monoclonal gammopathy and skin changes; s/p, status
post.
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Title Annotation:Original Article
Author:Marshall, Hyejong Song; Milikowski, Clara
Publication:Archives of Pathology & Laboratory Medicine
Article Type:Report
Date:Sep 1, 2017
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