Implementation of pre-captured videos for remote cytological evaluation of salivary gland lesions

Abstract

Objective

The objective of this study was to examine the feasibility of implementing videos captured by static telecytological applications for remote cytological evaluation of fine needle aspiration specimens from salivary gland lesions.

Methods

The current study was carried out on 102 fine needle aspiration specimens from salivary gland lesions with histological confirmation (benign lesions, 11; benign neoplasms, 68; malignant neoplasms, 23), retrospectively selected from the department’s registry. Videos were transferred via file transfer protocol to password-protected accounts for remote review by three independent cytopathologists. In addition to diagnosis, reviewers commented on overall digital video quality. Contributor’s and reviewer’s diagnoses were collected, recorded and statistically evaluated.

Results

Statistical evaluation of cytological diagnoses detected no significant difference in diagnostic accuracy between the diagnoses proffered on the basis of pre-captured videos and conventional slides. The overall interobserver agreement was ranging from substantial to almost perfect with κ values of 0.71–0.89.

Conclusions

Video production by static telecytology applications can be used as an alternative method for telecytological diagnosis of salivary gland fine needle aspirations. Videos of salivary gland fine needle aspirations can be used for rapid and accurate diagnosis, by diminishing turn-around times and improving the quality indices of small cytology departments. They can also be used for archiving, teleconsultation, educational and second opinion purposes, improving the performance of the already existing static telecytology stations.

Keywords

Telecytology salivary glands fine needle aspiration quality control telemedicine

Introduction

Telecytology is the interpretation of cytology material at a distance using digital material (images or videos).^1–7 Telecytology can be used for teaching, professional assessment, auditing, archiving, quantitative cytology and research, obtaining expert opinions on difficult cases, and routine diagnosis of the entire laboratory workload.^1–3,6,7 Telecytological diagnosis can be achieved either with the use of cytological pictures viewed in real time from the microscope (dynamic telecytological systems) or with the use of cytological pictures that are first captured in a digital format and then transmitted using a store-and-forward approach to distant observers (static telecytological systems).^1–5

In its simplest form, a static system comprises of a digital microscopic workstation comprising of microscope attached to a camera and a computer with high processing capacity and modem or Internet connections. Digital images are transferred via ﬁle transfer protocol to speciﬁc password protected accounts, via secure hypertext protocol using a 40-bit encrypted server on the world wide Web via an adaptable telepathology video management system or via multipurpose internet mail extensions (MIME)-encapsulated e-mail attachments.^1–3,6,7

Diagnoses made using telecytology should be as reliable as those made using conventional microscopy. The existing studies which focused on the possible impact of static telecytology in the everyday laboratory’s workflow have found a high concordance between telecytological and glass slide diagnoses.^1–4

Until 2018, many fine needle aspiration (FNA) reports from heterogeneous salivary gland tumours, with overlapping cytological features could not be accurately classified in distinct diagnostic categories, partly because of factors such as the lack of a widely accepted standardised reporting format and the use of multiple, often overlapping, cytological terms in descriptive reports lacking a definite diagnosis.^8–10

The Milan System for Reporting Salivary Gland Cytopathology (MSRSGC) was introduced in 2018 by the American Society of Cytology and the International Academy of Cytology in order to standardise terminology used in reporting salivary gland cytology.^8–10 This Milan System for Reporting Salivary Gland Cytopathology is based on the experience of experts in the field of cytopathology and on evidence from the literature. The seven categories used (non-diagnostic (ND), non-neoplastic (NN), atypia of undetermined significance (AUS), benign neoplasm (BN), salivary gland neoplasm of uncertain malignant potential (SUMP), suspicious for malignancy (SM) and malignant (M)) are supplemented by a list of diagnostic criteria. Besides classification, a precise identification of the neoplasm should also be indicated, as well as a clear distinction between low-grade (LG-M) and high-grade (HG-M) malignancies.^8–10

Until now, all available studies compare static and dynamic telecytology systems, but there is no study available that has focused on the alternative implementation of videos, captured by static telecytology stations for remote cytological diagnosis of salivary gland lesions. The present study aims to evaluate the diagnostic reproducibility of telecytology diagnoses in salivary gland FNAs among three cytopathologists using representative videos captured by an already existing static telecytology station. Diagnostic reproducibility was estimated by measuring interobserver and intraobserver agreement among participants and between telecytological and conventional light microscopy diagnoses. In addition, we have examined the possible impact of video quality on the reliability of telecytological diagnoses.

Materials and methods

The current study was carried out on 102 FNA specimens from salivary gland lesions with histological confirmation, retrospectively selected from the department’s registry.

The material initially collected by fine needle aspiration was prepared by the ThinPrep2000 automated slide processor (CytycCo., now Hologic, Bedford, Massachusetts, USA). From each case, one slide was prepared, stained by the May Grunwald-Giemsa (MGG) method, and examined by three independent board-certified cytopathologists. Conventional light microscopy was performed individually on an Olympus CX 31 microscope. The initial cytological diagnoses, made by conventional light microscopy, were made separately by each participant. In case of any major discrepancy, the final diagnosis was made after consultation and consensus of all participants. All cytopathologists used MSRSGC terminology and adhered to its diagnostic criteria. All participants were board-certified cytopathologists with documented previous experience in the field of static telecytology.

The initial cytological reports were kept for further statistical analysis (comparison with histology and measurement of intraobserver reproducibility between conventional cytology and telecytology made by pre-captured videos). The incidence of each Milan System category for reporting salivary gland cytopathology is summarised in Table 1.

Table 1.

Incidence of each Milan System category for reporting salivary gland cytopathology.

Diagnostic category	Incidence
I. Non-diagnostic (ND)	3/102
II. Non-neoplastic (NN)	18/102
III. Atypia of undetermined significance (AUS)	1/102
IVa. Neoplasm: benign (NB)	65/102
IVb. Neoplasm: salivary gland neoplasm of uncertain malignant potential (SUMP)	2/102
V. Suspicious for malignancy (SM)	1/102
VI. Malignant (M)	12/102

Histological reports were methodically collected, reviewed and compared with initial cytological diagnoses for all 102 cases. Malignancy rates for each MSRSGC category were calculated. The sensitivity and specificity of cytology for a histological diagnosis of malignancy were assessed. Statistical processing was performed with the software package IBM SPSS Statistics v.19 (IBM Corporation, Armonk, New York, USA).

Non-neoplastic lesions accounted for 12 of 102 cases (11.8%), whereas 90 lesions (88.2%) were neoplastic. Of the 90 neoplastic lesions, 66 (70%) were benign, and 24 (30%) were malignant. Correlation between cytological and histological diagnoses are summarised in Table 2.

Table 2.

Diagnostic correlation between cytology and histology reports.

	I	II	III	IVa	IVb	V	VI	Total
Pleomorphic adenoma	1	3		37	1		1	43
Monomorphic adenoma				2				2
Oxyphilic adenoma				1				1
Warthin's tumour		2		20				22
Abscess		2						2
Granulomatous sialadenitis	1	7						8
Retention cyst		1						1
Mucoepidermoid carcinoma		1	1	1	1		5	9
Adenoid cystic carcinoma	1	1		1			3	6
Carcinoma ex pleomorphic adenoma		1		3		1	2	7
Metastatic carcinoma							1	1
Total	3	18	1	65	2	1	12	102

Another cytopathologist collected all 102 glass slides and captured 1 representative videos from each case. Videos were captured with a Hamamatsu C4742-95 digital camera (Hamamatsu Photonics, Herrsching am Ammersee, Germany) mounted on an Olympus CX 31 microscope. The camera was connected via Small Computer System Interface (SCSI) interface to a 1200-MHz Pentium central processing unit (CPU) running Windows XP (Microsoft, Redmond, Washington, USA). Only one cytopathologist was assigned to capture one representative video from all cases, in order to ensure homogenization of the criteria applied in field selection. The person appointed to capture representatives videos possessed adequate diagnostic experience (had worked for 3 years as a certified cytopathologist and had made the diagnosis of 200 salivary gland FNAs) and had not participated in the initial diagnostic round in order to avoid any bias concerning field selection.

The videos captured were of 120 s duration each and provided valuable information that is routinely used in cytological diagnosis, such as background, cellularity, nuclear and cytoplasmic details. More specifically, the criteria usually adopted for the selection of the captured areas were high cellularity, absence of obscuring factors, excellent preservation and visualization of nuclear and cytoplasmic details, background details (necrosis or inflammation), inflammatory changes, reactive cellular changes, cytological atypia or dysplasia (when present). The area covered by each video was about 25% of the slide area. All videos contained areas of both 100× and 400× magnification. The videos magnification was changing during video capture in order to focus to specific areas of interest. The intention of the study was to provide to all participating cytopathologists adequate digital material for making accurate diagnosis, without any methodological bias that could compromise the results of our study. All videos captured areas of interest at 100× and 400× magnifications with 1124 × 1120 resolution at 16-bit colour depth and 300 dpi.

At 12 and 24 months after video capture, all 102 collected representative videos were transferred via file transfer protocol to specific password-protected accounts and were reviewed remotely by the same three cytopathologists on workstations using the Google Chrome Web browser. All videos were accompanied by an electronic record of all crucial medical data that could have impact on the cytological diagnosis of all samples included in our study. Reviewers commented on overall video quality using a 10-step scale, from 1 = very poor to 10 = excellent. Reviewers had adequate experience to work with digital material and to use Internet applications for diagnostic purposes.

The diagnostic approach of videos concerning criteria of diagnosis, terminology of lesions, requirements of adequacy and recommendations for further management were similar to those applied in conventional cytology (MSRSGC).^8–10

A detailed discussion of diagnostic criteria was not conducted between the cytopathologists, but all available clinical information was provided to all participants. Diagnostic categories and their subclassification are presented in Table 3.

Table 3.

Major cytological diagnostic categories for assessment of salivary gland lesions.

Classification	Diagnostic categories according to the Milan System for Reporting Salivary Gland Cytopathology
I. Non-diagnostic	Diagnostic category I
II. Benign: negative for malignancy, benign neoplasm or cell atypia	Diagnostic category II
III. Cell atypia	Diagnostic category III
IV. Benign neoplasm	Diagnostic category IVa
V. Suspicious for malignancy	Diagnostic categories IVb, V
VI. Malignant neoplasm	Diagnostic category VI

Cohen’s kappa statistic was used for the calculation of intraobserver reproducibility. Mean intraobserver reproducibility was calculated as the weighted average of the individual kappa values. To determine the significance of the intraobserver k values, we used the Svanholm formula.11,12 [Please check the points about kappa statistics – is k meant to be the kappa statistic, as j is used in the following paragraph?]

To assess interobserver agreement among cytopathologists for different diagnostic categories, kappa (j) statistics, first introduced in 1960, which provide a measure of agreement between two observers, was applied. Since our study involves more than two observers, a modification of kappa statistics allowing the comparison of more than two observers providing nominal (i.e. not ordered) answers, first proposed by Fleiss in 1971, was used.^11,12

The agreement is the total or the proportional number of cases in which the same diagnosis was issued between or within observers, including the part of the agreement that may be attributed to chance. The kappa statistic measures reproducibility, which is part of the agreement that cannot be explained purely by chance. Within the positive kappa values and in accordance with the study by Landis and Koch,¹² the agreement was interpreted as follows: a range of 0.00–0.20 indicates slight agreement, a range of 0.21–0.40 indicates fair agreement, a range of 0.41–0.60 indicates moderate agreement, a range of 0.61–0.80 shows very good agreement, while a range of 0.81–1.00 indicates excellent or almost perfect agreement. Interpretation of kappa values is presented in Table 4.

Table 4.

Interpretation of kappa values.

<0	Poor agreement
0.0–0.20	Slight agreement
0.21–0.40	Fair agreement
0.61–0.80	Substantial agreement
0.81–1.00	Almost perfect agreement

Results

The study was performed on representative videos captured from a total of 102 salivary gland FNAs that were transferred via file transfer protocol to password-protected accounts for remote review by three independent cytopathologists. The videos were examined by the same three cytopathologists three times (during initial diagnostic round, after 12 and after 24 months).

Intraobserver reproducibility between light microscopy diagnoses and telecytology diagnoses was calculated among all cytopathologists and ranged from perfect (for the more experienced cytopathologist) to nearly perfect (for the other less experienced cytopathologists) with the corresponding overall kappa values ranging from 0.71–0.82 (Table 5).

Table 5.

Intraobserver agreement between conventional cytological and telecytological diagnoses (kappa values).

Conventional cytological diagnosis versus	Kappa value
Conventional cytological diagnosis versus	1st diagnostic round	2nd diagnostic round	3rd diagnostic round
Cytopathologist 1’s telediagnosis	0.72	0.74	0.74
Cytopathologist 2’s telediagnosis	0.71	0.73	0.77
Cytopathologist 3’s telediagnosis	0.74	0.78	0.82

For all diagnostic categories, p<0.0001.

Interobserver reproducibility of telecytology diagnoses for each diagnostic category was calculated among all cytopathologists, during all three diagnostic rounds and ranged from substantial (for the more experienced cytopathologist) to nearly perfect (for the other less experienced cytopathologists) with the corresponding overall kappa values ranging from 0.71–0.91 (Table 6).

Table 6.

Interobserver reproducibility of telecytology diagnoses for each diagnostic category.

Diagnostic categories (2018 B Milan System for Reporting Salivary Gland Cytopathology )	Kappa value
	Initial diagnostic round	2nd diagnostic round (after 12 months)	3rd diagnostic round (after 24 months)
I. Non-diagnostic (ND)	0.81	0.82	0.83
II. Non-neoplastic (NN)	0.77	0.75	0.79
III. Atypia of undetermined significance (AUS)	0.72	0.70	0.73
IVa. Neoplasm: benign (NB)	0.74	0.76	0.78
IVb. Neoplasm: salivary gland neoplasm of uncertain malignant potential (SUMP)	0.70	0.71	0.73
V. Suspicious for malignancy (SM)	0.79	0.81	0.82
VI. Malignant neoplasm	0.89	0.89	0.91

Furthermore, the reviewers also commented on overall digital video quality. Reviewers’ opinion of video quality ranged from very good to excellent (Table 7).

Table 7.

Estimation of video quality.

Image quality	CYT 1	CYT 2	CYT 3
10	65	77	67
9	13	7	9
8	12	3	7
7	4	6	3
6	5	6	4
5	2	1	2
4	1	1	5
3		1	3
2			2
1
Total	102	102	102

CYT: cytopathologist.

Discussion

Modern cytopathology laboratories have to provide results of high quality and credibility. Over the last decade, the practice of clinical cytopathology was dramatically influenced by the broad implementation of informatics and computer sciences into the laboratory workflow. Cytopathology laboratories wishing to achieve an automated and seamless workflow process, to diminish turn-around times and improve their diagnostic accuracy have successfully adopted information technologies and automation. New types of cameras and microscopes, connected to computers made possible image capture and transmission (telecytology).^1–3,13

A telemedical application is a valuable tool for cytopathologists to manage and promote interlaboratory collaboration. The result is better cytological data management and sharing.^1–3,13

Preoperative diagnosis can guide the decision for surgery and extent of resection. Surgery is often not indicated for non-neoplastic salivary gland lesions, for metastatic cancer and malignant lymphoproliferative disease.^8–10 FNA consists of a well-recognised safe, accurate and cost-effective method for an immediate evaluation of salivary gland lesions which can improve and facilitate clinical management of patients by providing valuable information concerning the nature of the lesion examined.^8–10

MSRSGC, which was adopted in 2018, is an excellent tool for the diagnosis and management of salivary gland lesions. Its main objective is to improve communication between clinicians and cytopathologists and facilitate overall patient management. It is an evidence-based system, which provides clinical management strategies for each category. MSRSGC has classified salivary gland cytological diagnoses into seven categories; ND, NN, AUS, NB, SUMP, SM, M with an estimated risk of malignancy of 25%, 10%, 20%, 5%, 35%, 60% and 90% for each category.^8–10

The current study included patients with palpable and non–palpable salivary gland masses referred to Alpha Prolipsis Cytology Laboratories. The laboratory employs three board-certified cytopathologists with well-documented experience in salivary gland cytology. Since April 2018, Alpha Prolepsis Cytology Laboratories started reporting all salivary gland FNAs using the Milan system. They followed the guidelines in the diagnostic manual The Milan System for Reporting Salivary Gland Cytopathology.^8–10

Our laboratory is accredited since 2012, according to EN ISO 15189:2012. According to this international quality standard, as long as the number of mistakes committed during specimen collection, preparation and diagnostic interpretation diminishes, all monitored quality assessors continue to improve, and vice versa.^1–5 The laboratory is continuously monitoring factors, such as interobserver and intraobserver agreement, which play a crucial role in diagnostic reproducibility. The use of static telecytology applications for internal quality control purposes was proved an excellent alternative method for expert opinion acquisition in diagnostically challenging cases.^1–3,13

The slides collected for the production of the digital material from the Cytology Department’s registry were coming from already histologically confirmed cases. The histological examination provides the best way that cytology slides can be validated.^1,2 Inadequate validation of test slides could lead to indiscriminate failure of qualified, competent personnel participating in external quality control programmes.^1–3

The routine practice of telecytology may take place between a cytopathologist and another cytopathologist in a remote location.^1–5,14 Static telecytology systems capture cytologic pictures in a digital format followed by transmission to a distant observer. In its simplest form, a static system comprises of a digital microscopic workstation comprising of microscope attached to a camera and a computer with high processing capacity and modem or Internet connections.^1–5,14 The main disadvantages of static telepathology relate to the fact that the consulting telepathologist has no remote control of the microscope or imaging device/camera, their interpretation is limited to only captured field of views.^1,2,5,14 Static telecytology systems are used for evaluation of highly selected static images focusing only on few cells that may not show the entire evidence that is required for cytologic diagnosis.^1–,4,13,14 Pre-captured videos ensure continuity of cytological observation and provide substantial evidence of the representativeness of the selected fields.¹

The static telecytology systems have the advantage of considerably lower cost, but they only allow the capture of a selected subset of microscopic fields.^1,4,5,14,15 In diagnostically non-challenging cases, the bias in the selection of representative areas may have no implications. However, in difﬁcult instances, the potential bias of inexperienced personnel in acquiring and sending representative images may endanger accurate telecytological diagnosis.^1–3 On the other hand, the dynamic telecytology systems permit evaluation of the cytological material present on a slide.^1–4,15,16 However, these systems may be hampered by high network traffic, and their high cost of purchasing and maintaining may be unaffordable by small laboratories wishing to take advantage of such techniques for teleconsultation purposes.^1,2,16

Disadvantages of static telepathology relate to the fact that the consulting telepathologist has no remote control of the microscope or imaging device/camera, their interpretation is limited to only captured field of views.^1,4,5,14,15 Static telecytology systems are used for evaluation of highly selected static images focusing only on a few cells that may not show the real evidence that is required for cytologic diagnosis.^1,2,14,15

The use of static telecytology (by means of pre-recorded videos) for teleconsultation purposes in the laboratory’s daily workflow will further ensure the accuracy of preoperative cytological diagnoses and will contribute to cytopathologists continuous education and better understanding of the criteria applied in salivary gland lesion cytomorphological diagnoses.¹

Our results suggest that the level of concordance between telecytological and light microscopy diagnosis on a static telecytology consultation service (using pre-captured videos) may be as high as 85%. To our knowledge the magnification used for the videos production was a contributing factor to high interobserver agreement.¹ All videos used in our study were of high quality. In real life high quality images may not always be used, thus lowering results. High video quality was crucial for correct telecytological diagnosis. The maximum quality of the captured videos was ensured by continuous monitoring of imaging variables such as sharpness, contrast, colours and magnification. In our study, the cytopathologist appointed to capture the representative videos from each slide had enough experience to select the most representative regions from each slide examined.¹

In our laboratory, the person assigned to capture and transmit the images is an already board-certified cytopathologist with adequate experience in the cytological diagnosis of cervical smears. Less specialised personnel, such as inexperienced screeners, may endanger the acquisition of representative videos from each cytological slide. In such cases, the implementation of a well-documented standardised operational procedure would reduce risks of non-representative acquisition of digital material used for further telecytological diagnosis.

During diagnostic interpretation of cytological specimens by means of pre-captured videos, the cytopathologist has to implement the same diagnostic criteria used during conventional microscopy. The morphology of conventional and liquid-based cytology slides presents many similarities that allow accurate diagnosis in the majority of the cases examined. Some background details or cellular size differences between conventional and liquid-based cytology slides are well known to well-trained cytopathologists and already well described in cytopathology textbooks. In order to give some examples, we provide some images from diagnostically challenging cases, included in our study (Figures 1 –4).

Figure 1.

Adenoid cystic carcinoma, May Grunwald-Giemsa (MGG) stain, magnification ×400.

Figure 2.

Spindle cell pleomorphic adenoma, May Grunwald-Giemsa (MGG) stain, magnification ×400.

Figure 3.

Pleomorphic adenoma, May Grunwald-Giemsa (MGG) stain, magnification ×400.

Figure 4.

Warthin’s tumour, May Grunwald-Giemsa (MGG) stain, magnification ×400.

Telecytology by means of pre-captured videos, when integrated into the daily work flow, can provide special consultation opportunities to distant laboratories.^1,2,14 We suggest that static telecytology systems are preferred because of their low cost by laboratories that cannot afford the high cost of buying and maintaining dynamic systems. In addition, the telecommunication costs for the operation of static systems is lower as the usual common Asymmetric Digital Subscriber Line (ADSL) Internet connection is adequate to operate a static system.^1–3,14

Telecytology may be difficult to integrate into daily workflow.^1–3 Distant cytopathology departments with high needs for assistance in the form of expert consultation can rarely afford the high cost of buying and maintaining dynamic systems.^1–4 Static telecytological systems are affordable by all cytology departments and give the additional opportunity to all scientific personnel to participate in external quality control programmes, even when there is a significant time difference among participating laboratories.^1–4

Rapid telecytological diagnosis by means of pre-recorded videos can be used for diminishing turn-around time, a quality indicator that refers to the time between specimen collection and final cytological report submission.¹ The implementation of static telecytology into daily laboratory workflow will ensure the reproducibility of cytological diagnoses and make possible the production of digital educational material. As is well known, continuous education of medical personnel is a parameter of quality assessment.^1,2 The production of digitised educational material can be proved valuable in inter- or intra-laboratory proficiency testing programmes.^1–3,17

Last but not least, digital video storage and transmission must follow strict regulations in order to avoid any unauthorised alteration or improper use. Current standards of electronic medical data handling are still informative, yet the need for a secure electronic environment, especially in the field of static telecytology, continues to grow.^{1,4,5,14,17–20}

Conclusions

Our study suggests that cytological diagnoses made on the basis of pre-captured videos (from salivary gland FNAs prepared by means of liquid-based cytology) can be as reliable as those of conventional cytology. The diagnostic reliability of this method enables its use for further upgrading of static telecytology stations services, by producing digital virtual videos for quality assurance and educational purposes. Teleconsultation by means of pre-captured videos can be used as a valid quality assurance method of cytological diagnoses, especially in diagnostically challenging cases. Pre-captured videos can be used in proficiency testing programmes for assessing the diagnostic expertise of the laboratory’s medical staff.

The diagnostic reliability of static telecytology provides the potential for further amelioration of the laboratory services, by producing digital educational material for use in Web-based training systems. Those programmes can improve the professional skills of the participating medical staff and make them feel more confident in their daily work.

The adoption of standards for video file format that meet the needs of applications in cytopathology will enable the growth of these diagnostic applications in the near future. Standardization of the equipment used for video storage and transmission among distant cytology laboratories is indispensable for further implementation of such applications for consultation, analysis or conferencing purposes.

Future research must focus on the details of the implementation of a static telecytological application (with pre-captured videos) for proficiency testing purposes. That is, determining the required testing interval, elucidating the validation criteria applied to electronic material used for proficiency testing purposes and possibly changing the focus of the test from individuals to laboratory level testing.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship and/or publication of this article.

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