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Concordance Between Telepathologic Diagnosis and Conventional Histopathologic Diagnosis
A Multiobserver Store-and-Forward Study on 20 Skin Specimens
D. Piccolo, MD;
H. Peter Soyer, MD;
W. Burgdorf, MD;
R. Talamini, MD;
K. Peris, MD;
L. Bugatti, MD;
V. Canzonieri, MD;
L. Cerroni, MD;
S. Chimenti, MD;
G. De Rosa, MD;
G. Filosa, MD;
R. Hoffmann, MD;
I. Julis, MD;
H. Kutzner, MD;
L. Manente, MD;
C. Misciali, MD;
H. Schaeppi, MD;
M. Tanaka, MD;
W. Tyler, MD;
B. Zelger, MD;
H. Kerl, MD
Arch Dermatol. 2002;138:53-58.
ABSTRACT
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Objective To study the validity and feasibility of transferring images of cutaneous
biopsy specimens via e-mail to remote physicians active in dermatopathology
for teleconsultation.
Design Twenty skin specimens previously diagnosed at the Department of Dermatology,
University of Graz, Austria, were subsequently sent for teleconsultation using
the store-and-forward method. For each case, 3 or 4 images at different magnifications
were sent by e-mail to 16 colleagues (11 dermatopathologists and 5 pathologists)
in 15 centers in 6 different countries. Six weeks later each observer received
the hematoxylin-eosin–stained specimens to render a conventional diagnosis.
Setting Dermatopathology and pathology units within institutional and private
settings.
Material Twenty small skin biopsy specimens of cutaneous diseases were selected
randomly from a study set of 80.
Main Outcome Measure Concordance between telepathologic diagnoses and conventional histopathologic
diagnoses of 20 skin specimens.
Results On average, 78% of the telediagnoses were correct (range, 60%-95%),
whereas 85% of the conventional diagnoses were correct (range, 60%-95%). A
perfect diagnostic concordance was obtained in 7 (35%) of 20 cases, and a
significant difference was identified in only 1 case.
Conclusions Results suggest that telepathology performed by physicians active in
dermatopathology may serve as a reliable technique for the diagnosis of cutaneous
diseases when experts in dermatopathology are not available locally. Furthermore,
teledermatopathology is attractive because it provides an opportunity to obtain
timely consultation on difficult cases.
INTRODUCTION
IN RECENT years, continuous progress in computer technology has led
to the introduction of a revolutionary diagnostic tool known as telemedicine.1-3 Telepathology is defined as the practice of pathology at
a distance, by visualizing an image on a monitor rather than viewing a specimen
directly through a microscope.4-14
Using relatively simple equipment, dermatologists can rapidly transmit
microscopic still images photographed at one site to remote centers to obtain
a diagnostic consultation. Today's technologies allow a transfer of histopathologic
images in both dynamic (real-time) and static (store-and-forward) systems.
The first method provides remote consultation via a robotic microscope, which
can be controlled by the consulting pathologist. The equipment used for robotic
systems is relatively expensive and requires high data transmission rates
to achieve real-time image transfer. Using the store-and-forward method, each
image is captured and transmitted as a single file. The fields to be examined
are selected by the referring pathologist and then transmitted. This system
is much less expensive and does not require high-speed data transmission capability.
A limited number of studies have addressed the validity of both these systems,
and results suggest that static-image telepathology may be less accurate.15-20
A number of studies have demonstrated that teledermatology represents
a useful diagnostic tool, especially in communities where dermatologic services
are not available.21-29
Our group has published 2 studies demonstrating the reliability and reproducibility
of store-and-forward teledermoscopy for the diagnosis of pigmented skin lesions.30-31 In contrast, only a few teledermatopathology
studies have been done.10, 19
We report the results of a multicenter teledermatopathologic study on
20 cutaneous specimens. A total of 67 JPEG (joint photographic experts group)
compressed representative static images were sent by e-mail from Graz, Austria,
to 16 telepathologists around the world (Austria, Czech Republic, Germany,
Italy, Japan, and the United States). Each participant rendered a telepathologic
diagnosis for each case. After 6 weeks, all participants received representative
hematoxylin-eosin–stained specimens of each case and rendered another
diagnosis. Comparing these diagnoses allowed us to evaluate the concordance
between the telepathologic and conventional diagnoses.
MATERIALS AND METHODS
ON-SITE SAMPLING AND ANALYSIS
Our study included 20 histopathologic biopsy specimens of cutaneous
diseases selected randomly from a study set of 80. We concentrated on small
tissue specimens to avoid sampling error. Essential clinical information,
the number of images sent for each case, and the final diagnoses are given
in Table 1. The clinical information
was included on the actual histopathology laboratory submission form. For
example, for case 1, a trichofolliculoma, the clinical information read "59-year-old
female with a lesion on the forehead clinically diagnosed as sebaceous hyperplasia."
In most cases, the information was scant. All original histopathologic specimens
were examined with a conventional microscope (BX50; Olympus, Tokyo, Japan)
at the Department of Dermatology in Graz by 2 expert dermatopathologists (H.
Kerl and H.P.S.). One of them selected the fields to be photographed from
the original specimen and chose the magnification level. The final diagnosis
for these cases was made by both of the expert dermatopathologists in Graz
by assessing clinical features and histopathologic findings.
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Table 1. Clinical Data, Number of Images Sent for Each Case, Final
Diagnosis, and Number of Correct Telediagnoses and Conventional Diagnoses
for the 20 Cases
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TELECOMMUNICATION METHODS
Images were captured with a digital Kodak DCS 460 camera (Eastman Kodak
Co, Rochester, NY), which uses a Nikon N90 body (Tokyo, Japan) mounted on
an ordinary Olympus BX50 microscope. Each image was obtained with the digital
camera in PICT format file (Macintosh native graphics format). For each case,
images at 3 or 4 different magnifications were acquired (Figure 1). The original size of these images was 17 megabytes, 2036
x 3060 pixels (71.83 x 107.96 cm; 72 pixels per inch [ppi]), in
RGB color mode (36 bit). Successively, all images were subsampled to a size
of 511 x 768 pixels (18.02 x 27.08 cm; 72 ppi) in RGB color mode
(24 bit) and compressed by using JPEG compression at a fixed quality setting.
The software used for subsampling and compression was Adobe Photoshop 4.0
(Adobe, San Jose, Calif); the JPEG quality setting was set at 6 (this value
is proportional to compression ratio). Finally, compressed images had a mean
size of 53 kilobytes (kb) (range, 48-67 kb). This compression was required
to allow a faster e-mail transmission. All images were sent to the remote
centers via e-mail (Eudora Light, San Diego, Calif) together with basic patient
data (age, sex, site and duration of the lesion, and clinical diagnosis).
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Compressed JPEG images of case 1 (trichofolliculoma) at different
original magnifications: A, x4; B, x10; and C, x40.
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STATISTICAL ANALYSIS
The  2 test and Fisher exact test were used for quantitative
parameters. Results were considered statistically significant at P .05 (2-sided).32
RESULTS
The clinical data, number of images, final diagnosis by both the expert
dermatopathologists in Graz, and the number of correct telediagnoses and correct
conventional diagnoses for the 20 cases are given in Table 1. A diagnostic concordance between the telediagnoses and
conventional diagnoses of the 16 pathologists was obtained in 7 (35%) of 20
cases (cases 1, 4, 8, 11, 16, 18, and 19). A significant difference between
telediagnoses and conventional diagnoses was identified in only 1 case (case
20). Telediagnoses were superior to conventional diagnoses in 4 (20%) of 20
cases (cases 2, 10, 13, and 14), whereas in 9 (45%) of 20 cases (cases 3,
5, 6, 7, 9, 12, 15, 17, and 20), telediagnoses were inferior to conventional
diagnoses.
The performance of each participant is summarized in Table 2. Detailed results on telepathologic diagnosis, conventional
histopathologic diagnosis, and concordance between these 2 methods for each
of the 20 skin specimens is given for each independent observer. If the same
incorrect diagnosis was made on both telediagnosis and conventional diagnosis,
this is interpreted as "agreement." For example, observer 1 made 16 correct
telediagnoses and 19 correct conventional diagnoses, but only 15 diagnoses
were concordant. Thus he or she changed all 4 incorrect telediagnoses, but
also changed 1 correct telediagnosis. On average, 78% of the telediagnoses
were correct, with a range from 60% to 95%, whereas conventional diagnoses
were correct 85% of the time (range, 60%-95%). Differences of 10% or less
from perfect agreement were found among 11 (69%) of 16 observers (observers
2, 3, 4, 7, 8, 10, 11, 13, 14, 15, and 16). Differences greater than 10% to
15% occurred among 4 observers (25%; observers 1, 6, 9, and 12), whereas for
only 1 observer (6%; observer 5) was the difference from perfect agreement
more than 15%. No statistical differences were found comparing the percentage
of perfect agreement between telediagnoses and conventional diagnoses for
each observer (P>.05).
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Table 2. Results of Telepathologic and Conventional Histopathologic
Diagnoses and Their Concordance on 20 Skin Specimens According to 16 Independent
Observers
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Table 3 summarizes detailed
data on telepathologic diagnoses and conventional histopathologic diagnoses
of all 20 skin specimens. It allows one to identify which diagnoses were proposed
in addition to the final diagnosis.
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Table 3. Detailed Data on Telepathologic Diagnoses and Conventional
Histopathologic Diagnoses*
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COMMENT
In this study, we evaluated the influence of image selection on diagnostic
performance to verify concordance between conventional diagnosis and telediagnosis.
The results obtained showed that telepathology accuracy was slightly lower
than glass slide accuracy (78% and 85%, respectively). Nevertheless, among
15 (94%) of 16 observers, no significant differences in accuracy were found
between telepathology and conventional pathology, suggesting the usefulness
of teledermatopathology.
Telepathology involves the use of the new telematic technologies to
transmit images for the purposes of diagnosis, consultation, and education.
In the past years, many articles on telepathology have been published.4-20
Moreover, many Web sites teaching with telepathology can be found easily with
the common search engines. The major problem using e-mail is that the security
and confidentiality of the patient data may be compromised by hackers.11
The main problems with static telepathology are image selection and
image quality. Image selection is more of a problem for the store-and-forward
system. It is important to emphasize that the referring pathologist must select
images that adequately present the case without attempting to influence the
remote pathologists. The main risk lies in a personal and incomplete photographic
characterization of the case on the basis of a diagnostic hypothesis, inadvertently
leading the remote pathologist toward a diagnostic misinterpretation. The
referring pathologist and the consultant should understand the risks involved
in embracing and using these technologies. The store-and-forward method should
be considered in small dermatopathology biopsy specimens where the sampling
bias is not a major problem. In a large solid tumor, for example, image selection
by the local pathologist could represent a greater obstacle.
Problems such as these might be avoided by using a remote-control telepathology
system, where the consultant pathologist controls the microscope, directly
choosing the areas of viewing and the magnification. One disadvantage, however,
of using the real-time systems is that they are more technologically complex
and expensive. Furthermore, the consultant pathologist must be online together
with the referring pathologist.
The quality of the histopathologic images depends on the equipment used
and the capacity of the telecommunications link. For our study, all 67 histopathologic
images were compressed using JPEG compression. As demonstrated by Okumura
et al33 in 1997 and by Kittler et al34 in 1998, with this type of compression the lost information
is most likely to be imperceptible to the individual doing the remote assessment.
The compression of the images was necessary to allow a faster e-mail transmission;
JPEG is an accepted standard image type for the multipurpose Internet mail
extension (MIME). This technology is an extension to the e-mail message format
facilitating the delivery of multimedia messages such as images, sounds, and
movies.
Making telepathologic diagnosis on a high-resolution monitor is qualitatively
different than directly viewing images through a conventional light microscope.
Becker et al35 demonstrated the importance
of experience in using a telepathology system both for accurate reading of
video images and for effective communication between sending and receiving
pathologists. The telepathologic diagnostic accuracy of many of these systems
is untested. Our study suggests that for small biopsy specimens, the sampling
procedure is not really problematic and that the store-and-forward method
works well.
In 5 cases (cases 4, 8, 11, 13, and 16), the telepathologic diagnosis
was identical to the final diagnosis established by clinicopathologic correlation,
whereas the conventional histopathologic diagnosis was the same as the final
diagnosis in 6 cases (cases 4, 5, 8, 11, 12, and 16). In 2 cases (cases 1
and 2), there was only a slight difference between telediagnoses and conventional
diagnoses compared with the final diagnosis. In case 1, three of 16 pathologists
preferred the diagnosis of trichoepithelioma instead of trichofolliculoma
not only when viewing transmitted images but also by conventional microscopy.
In case 2, two remote pathologists and 4 pathologists performing conventional
diagnosis made the diagnosis of xanthoma instead of xanthelasma. In cases
6, 7, and 9, only the combination of both clinical and histopathologic findings
permitted one to obtain the final diagnoses (pityriasis lichenoides for the
first case, Grover disease for the second, and Hailey-Hailey disease for the
third). On the basis of only the histopathologic features, many participants
diagnosed other bullous diseases such as pemphigus, Darier disease, herpesvirus
infection, and acantholytic dermatitis for cases 7 and 9 (Table 3). This result underscores the importance of meticulous clinicopathologic
correlation for the diagnosis of certain inflammatory skin diseases. Such
a clinicopathologic correlation could be achieved by evaluating a relevant
clinical image, something that could be integrated in a telepathology protocol.
This study is based on only 20 skin specimens. We have confirmed that
the store-and-forward method is a useful tool within the field of dermatopathology
at least when dealing with small biopsy specimens where sampling bias is not
a major obstacle. Particularly in inflammatory skin diseases, a meticulous
clinicopathologic correlation is still crucial for achieving competent diagnosis.
AUTHOR INFORMATION
Accepted for publication May 1, 2001.
Corresponding author: H. Peter Soyer, MD, Department of Dermatology,
University of Graz, Auenbruggerplatz 8, A-8036 Graz, Austria
(e-mail: peter.soyer{at}unigraz.at).
From the Departments of Dermatology of the University of L'Aquila,
L'Aquila, Italy (Drs Piccolo and Peris); University of Graz, Graz, Austria
(Drs Soyer, Cerroni, and Kerl); General Hospital, Jesi, Italy (Drs Bugatti
and Filosa); University of Tor Vergata, Rome, Italy (Dr Chimenti); Philipp
University, Marburg, Germany (Dr Hoffmann); BioLab Laboratory for Histopathology,
Prague, Czech Republic (Dr Julis); Gemeinschaftspraxis, Friedrichshafen, Germany
(Dr Kutzner); University of Bologna, Bologna, Italy (Dr Misciali); General
Hospital, Salzburg, Austria (Dr Schaeppi); Keio University, Tokyo, Japan (Dr
Tanaka); and University of Innsbruck, Innsbruck, Austria (Dr Zelger); from
Tutzing, Germany (Dr Burgdorf); the Departments of Epidemiology (Drs Talamini
and Filosa) and Pathology (Dr Canzonieri), Centro di Riferimento Oncologico,
Aviano, Italy; and the Departments of Pathology of the University Federico
II, Naples, Italy (Dr DeRosa); General Hospital S. Filippo Neri, Rome (Dr
Manente); and the Geisinger Medical Center, Danville, Pa (Dr Tyler).
REFERENCES
| |
1. Perednia DA, Allen A. Telemedicine technologies and clinical applications. JAMA. 1995;273:483-488.
FREE FULL TEXT
2. Allen A, Perednia DA. Telehealth revolution. ComNets. 1996;2:59-64.
3. Bashshur RL. On the definition and evaluation of telemedicine. Telemed J. 1995;1:19-30.
PUBMED
4. Weinstein RS, Bloom KJ, Rozek LS. Telepathology: long distance diagnosis. Am J Clin Pathol. 1989;91:S39-S42.
5. Oberholzer M, Fischer R, Christen H, et al. Telepathology with an integrated services digital network: a new tool
for image transfer in surgical pathology: a preliminary report. Hum Pathol. 1993;24:1078-1085.
PUBMED
6. Schwarzmann P, Schmid J, Schnorr C, Strassle G, Witte S. Telemicroscopy stations for telepathology based on broadband and ISDN
connections. Arch Anat Cytol Pathol. 1995;43:209-215.
PUBMED
7. Della Mea V, Forti S, Puglisi F, et al. Telepathology using Internet multimedia electronic mail: remote consultation
on gastrointestinal pathology. J Telemed Telecare. 1996;2:28-34.
PUBMED
8. Weinstein RS, Bhattacharyya AK, Graham AR, Davis JR. Telepathology: a ten-year progress report. Hum Pathol. 1997;28:1-7.
FULL TEXT
| PUBMED
9. Doolittle MH, Doolittle KW, Winkelman Z, Weinberg DS. Color images in telepathology: how many colors do we need? Hum Pathol. 1997;28:36-41.
PUBMED
10. Della Mea V, Puglisi F, Forti S, et al. Expert pathology consultation through the Internet: melanoma versus
benign melanocytic tumours. J Telemed Telecare. 1997;3 Suppl 1:17-19.
11. Agbamu DA, Sim E. The data security aspects of telepathology via the Internet have been
ignored. Hum Pathol. 1997;28:1440-1441.
PUBMED
12. Dervan PA, Wootton R. Diagnostic telepathology. Histopathology. 1998;32:195-198.
PUBMED
13. Almagro UA, Dunn BE, Choi H, Recla DL. Telepathology. Am J Surg Pathol. 1998;22:1161-1163.
PUBMED
14. Weinberg DS, Allaert FA, Dusserre P, et al. Telepathology diagnosis by means of digital still images: an international
validation study. Hum Pathol. 1996;27:111-118.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
15. Weinstein RS. Static image telepathology in perspective. Hum Pathol. 1996;27:99-101.
PUBMED
16. Dunn BE, Almagro UA, Choi H, et al. Dynamic-robotic telepathology: Department of Veterans Affairs feasibility
study. Hum Pathol. 1997;28:8-12.
FULL TEXT
| PUBMED
17. Halliday BE, Bhattacharyya AK, Graham AR, et al. Diagnostic accuracy of an international static-imaging telepathology
consultation service. Hum Pathol. 1997;28:17-21.
PUBMED
18. Weinstein LJ, Epstein JI, Edlow D, Westra WH. Static image analysis of skin specimens: the application of telepathology
to frozen section evaluation. Hum Pathol. 1997;28:30-35.
PUBMED
19. Berman B, Elgart GW, Burdick AE. Dermatopathology via a still-image telemedicine system: diagnostic
concordance with direct microscopy. Telemed J. 1997;3:27-32.
PUBMED
20. Afework A, Beynon MD, Bustamante F, et al. Digital dynamic telepathology: the virtual microscope. Proc AMIA Symp. 1998; :912-916.
21. Perednia DA, Brown NA. Teledermatology: one application of telemedicine. Bull Med Libr Assoc. 1995;83:42-47.
WEB OF SCIENCE
| PUBMED
22. Zelickson BD, Homan L. Teledermatology in the nursing home. Arch Dermatol. 1997;133:171-174.
FREE FULL TEXT
23. Gilmour E, Campbell SM, Loane MA, et al. Comparison of teleconsultations and face-to-face consultations: preliminary
results of a United Kingdom multicentre teledermatology study. Br J Dermatol. 1998;139:81-87.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
24. Kvedar JC, Edwards RA, Menn ER, et al. The substitution of digital images for dermatologic physical examination. Arch Dermatol. 1997;133:161-167.
FREE FULL TEXT
25. Lesher JL, Davis L, Gourdin FW, English D, Thompson WO. Telemedicine evaluation of cutaneous diseases: a blinded comparative
study. J Am Acad Dermatol. 1998;38:27-31.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
26. Lowitt MH, Kessler II, Kauffman CL, Hooper FJ, Siegel E, Burnett JW. Teledermatology and in-person examinations: a comparison of patients
and physician perceptions and diagnostic agreement. Arch Dermatol. 1998;134:471-476.
FREE FULL TEXT
27. Norton SA, Burdick AE, Phillips CM, Berman B. Teledermatology and underserved populations. Arch Dermatol. 1997;133:197-200.
FREE FULL TEXT
28. Phillips CM, Burke WA, Shechter A, Stone D, Balch D, Gustke S. Reliability of dermatology teleconsultations with the use of teleconferencing
technology. J Am Acad Dermatol. 1997;37:398-402.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
29. Provost N, Kopf AW, Rabinovitz HS, et al. Comparison of conventional photographs and telephonically transmitted
compressed digitized images of melanomas and dysplastic nevi. Dermatology. 1998;196:299-304.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
30. Piccolo D, Smolle J, Wolf IH, et al. Face-to-face versus telediagnosis of pigmented skin tumors: a teledermoscopic
study. Arch Dermatol. 1999;135:1467-1471.
FREE FULL TEXT
31. Piccolo D, Smolle J, Argenziano G, et al. Teledermoscopy: results of a multicentric study on 43 pigmented skin
lesions. J Telemed Telecare. 2000;6:132-137.
PUBMED
32. Fleiss LJ. Statistical Methods for Rate and Proportions. 2nd ed. New York, NY: John Wiley & Sons; 1981:212-236.
33. Okumura A, Suzuki J, Furukawa I, Ono S, Ashihara T. Signal analysis and compression performance evaluation of pathological
microscopic images. IEEE Trans Med Imaging. 1997;16:701-710.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
34. Kittler H, Seltenheim M, Pehamberger H, Wolff K, Binder M. Diagnostic informativeness of compressed digital epiluminescence microscopy
images of pigmented skin lesions compared with photographs. Melanoma Res. 1998;8:255-260.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
35. Becker RL Jr, Specht CS, Jones R, Rueda-Pedraza ME, O'Leary J. Use of remote video microscopy (telepathology) as an adjunct to neurosurgical
frozen section consultation. Hum Pathol. 1993;24:909-911.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
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