Context

Telepathology is a particular form of telemedicine that fundamentally alters the way pathology services are delivered. Prior reviews in this area have mostly focused on 2 themes, namely technical feasibility issues and diagnosis accuracy.

Objectives

To synthesize the literature on telepathology implementation challenges and broader organizational and societal impacts and to propose a research agenda to guide future efforts in this domain.

Data Sources

Two complementary databases were systematically searched: MEDLINE (PubMed) and ABI/INFORM (ProQuest). Peer-reviewed articles and conference proceedings were considered. The final sample consisted of 159 papers published between 1992 and 2013.

Conclusions

This review highlights the diversity of telepathology networks and the importance of considering these distinctions when interpreting research findings. Various network structures are associated with different benefits. Although the dominant rationale in single-site projects is financial, larger centralized and decentralized telepathology networks are targeting a more diverse set of benefits, including extending access to pathology to a whole region, achieving substantial economies of scale in workforce and equipment, and improving quality by standardizing care. Importantly, our synthesis reveals that the nature and scale of encountered implementation challenges also varies depending on the network structure. In smaller telepathology networks, organizational concerns are less prominent, and implementers are more focused on usability issues. As the network scope widens, organizational and legal issues gain prominence.

Telepathology is defined by the American Telemedicine Association as “the electronic multimedia communication across a network of pathology-related information, between 2 or more locations for use-cases between pathologists and/or qualified laboratory personnel, and may include involvement by clinicians and/or patients.” 1  This particular form of telemedicine has several applications. First, a distant pathologist can provide a primary diagnosis to a site with no pathologist. Within that category, intraoperative examination enables a diagnosis to be provided immediately during surgery. Second, a pathologist can request a second opinion from a distant colleague for a complex or ambiguous case, or an expert referral from a subspecialist. Third, other telepathology applications include quality assurance, education, and research. Telepathology is a rapidly growing segment of the telemedicine field. The global telepathology market totaled nearly $2.1 billion in 2012. According to a recent report, this market is expected to grow at a compound annual growth rate of 14.7% from$2.2 billion in 2013 to nearly \$4.5 billion in 2018.2

Prior research on telepathology has focused on 2 important themes. The first concerns technical feasibility issues such as image quality, bandwidth, hardware selection, and information technology (IT) architecture.3,4  The second theme refers to diagnosis accuracy, that is, “how accurate are all diagnoses made via telemedicine, and how does this level of accuracy compare with diagnoses made through conventional medical care.” 5  This stream of research suggests that telepathology diagnoses are acceptable, although no systematic reviews have been identified.6,7  See the study by Weinstein et al8  for a summary.

Although deepening our knowledge on these 2 topics remains important, we believe that nontechnical issues deserve more attention. A recent survey of IT practitioners by the Gartner Group9  suggests that technical skills were the main source of failure in less than 1% of IT projects versus 78% for organizational skills. And in the particular context of telepathology, Furness and Bamford10  noted that “as technology advances, and as prices fall, the main barrier to implementation is increasingly a resistance to change amongst the humans rather than the limitation of the machines.”

Telepathology, more than other forms of telemedicine, involves radical changes in workflows, clinical processes, and professional responsibilities. Unlike most forms of telemedicine, telepathology does not require the patient's presence, which makes it a more dematerialized and frequently asynchronous form of telemedicine. Teleradiology, telepathology's close cousin, does not require the patient's presence either, but radiologists' transition to digital perpetuates their practice of working with digital images, whereas pathologists traditionally examine physical artifacts. Tellingly, the physical slide still retains legal value and must be examined and archived in most jurisdictions. The transition to telepathology thus adds extra steps to the process and involves laboratory technicians performing tasks previously devolved onto pathologists, such as manipulating large pieces of tissues and specimens.

In light of the above, the primary objectives of this review article are twofold. We aim to synthesize the extant literature on the implementation challenges and impacts of telepathology and to propose a research agenda to guide future efforts in this domain. The remainder of this article is structured as follows. In the next section, the methods that guided the review process are detailed. Next, we present the profile of the studies included in our sample, and the main findings that emerged from a thematic analysis. In the Comment section, we propose a research agenda to orient future efforts in this growing field.

## MATERIALS AND METHODS

Scoping reviews aim to map the key issues underpinning a research topic and the main sources and types of empirical evidence available.11,12  They usually focus on breadth rather than depth of analysis, and their main strengths “lie in [their] ability to extract the essence of a diverse body of evidence and give meaning and significance to a topic that is both developmental and intellectually creative.” 13  Two complementary databases were searched: MEDLINE (PubMed) and ABI/INFORM (ProQuest). The following keywords were used: telepathology, digital microscopy, virtual microscopy, distance pathology, digital macroscopy, digital pathology, digital slide, virtual slide, and whole slide imaging. Only peer-reviewed articles and conference proceedings were considered. MEDLINE and ABI/INFORM returned 1248 and 167 papers, respectively. As mentioned earlier, our focus was on telepathology implementation challenges and impacts; hence, we excluded papers focusing on technical feasibility and diagnostic accuracy issues. As shown in Figure 1, the final sample consisted of 159 relevant papers published between 1992 and January 2013.

Figure 1.

Diagram of study selection process.

Figure 1.

Diagram of study selection process.

Data charting refers to a technique for synthesizing and interpreting qualitative data by sifting, charting, and sorting material.14  In this review, the first author coded all articles included in our sample using a reference management software program. The coding scheme was designed a priori to cover the objectives, methods, context, and nature of the papers. However, as Levac et al12  note, in scoping studies “the nature and extent of data to extract from included studies is unclear.” Therefore, following their recommendation, the authors modified iteratively the coding scheme to embrace field diversity rather than to reduce it. The studies included in our final sample are listed in Supplemental Table 1 (see supplemental material file at www.archivesofpathology.org in the December 2015 table of contents).

## RESULTS

### Profile of the Primary Studies

As shown in Table 1, interest in managerial telepathology research has risen steadily, with 22 of the papers (14%) in the sample published between 1992 and 1998, rising to 55 (35%) during the 1999 to 2005 period, and progressing to 82 (52%) between 2006 and early 2013. Publication outlets are diverse, with papers in our sample published in 64 distinct outlets, mostly in pathology (72; 46% of papers) and medical informatics (60; 38%) peer-reviewed journals. The topics addressed in those 2 parent disciplines are roughly similar in terms of frequency, suggesting the interdisciplinary nature of the topics and the relevance of a scoping review to synthetize the extant literature.

Table 1.

Profile of the Sample

The diversity of the sample is revealed by several indicators. First, 84 of the papers (53%) specifically focus on a context where telepathology is used for diagnoses (the sample did not allow a reliable distinction between primary and secondary diagnosis). A significant portion of the papers (42; 26%) address multiple or unspecified forms of telepathology applications, suggesting that even telepathology managerial research remains often driven by the telepathology artifact rather than by its purposes. Second, the nature of scientific evidence also varies widely, as shown in Table 1. For one thing, 60 papers (38%) included in our sample are conceptual, with no original empirical data. Further, 54 (34%) are descriptive case studies, providing an account of a telepathology project and the lessons and observations derived from it, typically with no specific research question being addressed. The relative importance of this group illustrates the still-exploratory nature of managerial telepathology research. Last, we count 45 evaluative studies (28%) that assess one or several aspects of telepathology in health care organizations.

Out of the 99 empirical papers, 42 (46%) do not explicitly describe the source of the evidence presented, especially in descriptive case studies, where knowledge usually stems from the authors' firsthand involvement in the project. Evaluation studies more systematically embrace a specific investigation method, with researchers using quantitative data, mostly from surveys, in half of the papers. The sample remains also largely atheoretical, with only 7 papers explicitly applying theories or conceptual models. For instance, Delone and McLean's IT success model was used to investigate technology impacts,15  and the Technology Acceptance Model helped explain telepathology adoption among pathologists.16  For its part, the theory of knowledge barriers was used to deepen our understanding of telepathology implementation challenges.17

Of utmost interest, diverse telepathology network structures emerged from our sample as shown in Figure 2. In single-location projects, slides are digitized for local use only. Most of these projects are educational telepathology, generally in teaching hospitals.18  Telepathology can also be set up in single sites for quality assurance purposes.19  In a one-to-one network, 2 health care organizations are connected such that a consulting site provides pathology services to a referring site. This network type is typical for experimenting with telepathology,20  providing quality assurance to a satellite organization,21  or substituting for a local or visiting pathologist.22,23  In a centralized network, a large institution usually provides pathology expertise to one or several smaller health care organizations. These are often more mature telepathology projects, such as a teaching hospital offering pathology consultations to sites located either in a remote region or in integrated health care systems such as the US Veterans Integrated Service Network.2426  Lastly, a decentralized network connects multiple locations with no single hub for consulting pathologists (point-to-point network). As an example, the Eastern Québec Telepathology Network in Canada aims at providing uniform diagnostic pathology services to pathologists and surgeons in a territory of 408 760 km2 with 1.7 million inhabitants where the density, in certain areas, is as low as 0.4 inhabitants/km. This network, one of the largest in the world, counts no single responding site to which community hospitals turn for pathology services. Rather, the architecture of the network was purposely designed to encourage decentralization and the development of a regional organization of pathology services.15

Figure 2.

Profile of telepathology network structures in various settings.

Figure 2.

Profile of telepathology network structures in various settings.

### Thematic Analysis

We now turn our attention to the main themes investigated in the selected articles, namely telepathology impacts and implementation challenges. Table 2 presents a summary of the coding process. Note that a single article may address more than one impact or benefit. For each topic, we summarize in the following paragraphs the main findings and underline key areas where we feel further research is needed.

Table 2.

Number of Articles Referring to Telepathology Impacts and Challenges

#### Telepathology Impacts

##### Accessibility of Care

Accessibility of care usually refers to the relative ease or difficulty in obtaining health services in the face of obstacles that can be geographic, economic, or social.27  Access to pathology is critical to enable diagnoses, of cancers for instance. The absence of a local pathologist and of telepathology is palliated by slow physical tissue transfer, roaming pathologists, and, when immediate diagnosis is needed, more aggressive surgeries or patient transfers to larger institutions. These alternatives can impair patient health, generate delays and costs, and constrain surgery options and planning.15

Pathologists are unevenly distributed, as the presence of full-time pathologists may not be justified in low–population-density areas, and interest in telemedicine in general and telepathology in particular is moderately related to population density.28  In fact, some of the earliest telepathology experiments were conducted to address this problem in sparsely populated areas such as northern Norway.29,30  Telepathology can improve access to pathology by (1) widening access to pathology services in regions underserved in pathology31 ; (2) preventing service loss when a pathologist leaves32 ; (3) providing a substitute when the local pathologist is absent, sick, or on vacation33 ; and (4) preventing service disruptions by sparing pathologists travel to remote locations.21

Pathologists are also unevenly distributed around the globe, with half of trained pathologists residing in the United States, serving less than 5% of the world's population.34  Telepathology has been used to provide pathology services to developing countries with no or limited access to pathology or subspecialty pathology.3437  Another key benefit is better access to consultations. This is true for isolated pathologists needing a second opinion, but also for those sending expert referrals to subspecialist pathologists.38  As the pathology discipline becomes increasingly specialized, advice from subspecialists, such as neuropathologists, becomes sought after.39,40  A case in point is the Union for International Cancer Control, which offers a worldwide service specializing in second opinions for tumor diagnostics.41

In the long run, telepathology may render pathology services and its subspecialties available 24/7 by routing cases at night to pathologists in different time zones,8,33  as can already be observed in some cases with teleradiology. Nevertheless, although improved accessibility to pathology and care in general is the major benefit claimed by telepathology implementers, especially in larger centralized and decentralized settings, empirical evidence for such impacts remains scarce and anecdotal.39,42

##### Quality of Care

Quality of care is generally addressed in the literature through the angle of diagnosis accuracy, with researchers investigating whether telepathology diagnoses are as good as the microscope-based gold standard. Nevertheless, telepathology adds direct and indirect clinical value of its own. First, improved access to pathology can lead to better care. Intraoperative telepathology examinations, for instance, allow less-numerous, more-timely, better-informed, and less-aggressive surgeries.26  Second, telepathology offers long-term unique potential for image treatment and aids to diagnosis, which promises to assist pathologists in their diagnostic work.43,44  Third, it facilitates quality assurance even for isolated pathologists.45  Finally, telepathology facilitates learning and expertise building. Explaining the diagnosis provides an educational benefit to the referring pathologist or surgeon.46  Competence building is even the main project goal in some developing countries' initiatives.36,47  But pathologists in reference centers also benefit from telepathology by accessing complex cases, because for “subspecialists to work together in a critical mass is essential for them to preserve their diagnostic and scientific acumen.” 20  Telepathology may thus play a key role in increasing pathologists' specialization.48  Compelling empirical evidence associated with these promises remains to be provided, though.

##### Efficiency

Only telepathology for educational purposes offers unambiguous evidence of simultaneous improved access (to learning materials) and improved quality (of students' learning and satisfaction) at a lower cost.49,50  For other applications, “telepathology slides, unlike the transition to digital radiology, have no immediate and readily identifiable payback that resonates with the holders of the purse strings.” 45  Economic benefits are difficult to monetize, and efficiency has rarely been investigated systematically.51,52  Some researchers even argue that profitability is not to be expected and should not be a goal.53  Nevertheless, there is increasing demand for economic evaluations of telemedicine projects.54

Hardware, software, and support contract costs are easy to monetize, and hence the most often cited, along with the costs of technicians, networks, and data storage.43,55,56  Telepathology can generate cost savings for health care organizations. The most prominent and widely cited savings is on pathologists' salaries when a full-time expert is not justified.22,39  Telepathology also enables economies of scale and optimization of resources such as laboratories, microscopes, and equipment, and the automation of certain repetitive activities in slide processing, cytology screening, or quality assurance.43,57,58  Finally, it can reduce courier and archiving costs, although this kind of gain is often downplayed as relatively minor, given that slides still need to be stored and archived for legal reasons.7,56

Telepathology renders access to patient files easier and faster, especially for case slide reconsultations and for pathology students.19,59,60  It can also reduce travel time for pathologists.57  From a revenue perspective, a few health care institutions have invested in telepathology to increase income generated by their leading specialists and to boost their staffing levels by reducing their travel time.17,21,52

Two main approaches have been used to investigate the efficiency of telemedicine projects, namely cost-effectiveness analyses and cost-benefit analyses.27,54  In a cost-effectiveness analysis, telepathology costs are compared with those of alternative solutions providing equal service, such as a courier service to send slides to another site or an onsite or a roaming pathologist.23,24,61,62  Findings, typically observed in one-to-one networks, suggest that profitability is context dependent. A long distance between 2 sites favors telepathology over courier, as does a medium level of activity.63  Low activity levels favor courier because of telepathology's high setup costs, whereas high activity levels may justify a resident pathologist.61  However, these analyses need to extend beyond one-to-one networks. Moreover, evolving technologies and decreasing IT costs mean that most findings are already obsolete.

By contrast, cost-benefit analysis is a value-added approach in which costs and benefits are comprehensively assessed using standardized measures, including operational elements of enhanced patient care. Benefits are maximized when the detected medical conditions have a high incidence, have high risk in case of early detection failure (or high benefits of early detection), and are not trivial (eg, tumors).5,56  The study by Isaacs et al56  is the only one that has used the cost-benefit analysis technique to assess telepathology benefits. More such analyses are required to account for improvement in accessibility of care, the key motivation for investing in such projects. A comprehensive and long-term approach to impact evaluation should also include changes in pathology laboratory workflows and in broader health care structures.44

##### Organization and Structure of Pathology Services

Last, researchers have also noted the potential impact of telepathology on health care structures. As pathologists team up to serve larger areas, pathology services will likely be concentrated into centralized laboratories.55,58,64,65  Enlarging health care networks may lead to the emergence of globalized diagnostic services.66,67  To small health care institutions, telepathology offers the potential to outsource pathology at lower cost, leveling the playing field by allowing smaller structures to use telepathology instead of hosting their own pathology service.21,51,68  Academic and other subspecialty practices may have ambivalent outcomes, as they will benefit from better use of their specialists but be financially affected negatively by increased competition and lowered prices.69

#### Telepathology Implementation Challenges

Once a decision to invest in telepathology has been made, clinicians and managers face a variety of implementation challenges beyond technical aspects. Indeed, telepathology projects represent sociotechnical changes that require overcoming a wide variety of challenges or barriers.17,70,71  Beyond technical issues, challenges can be found at the individual, organizational, and legal levels (see Table 2). Each of these categories will be discussed in turn.

##### Individual Barriers

Telepathology implementers need to ensure that targeted pathologists, technicians, and surgeons accept the new system and/or work environment. Many clinicians see the lack of clinical value as one of the primary barriers.45  Attitudes of pathologists towards telepathology have long been investigated, as shown by Callas et al.53  As in other forms of telemedicine, project champions play a key role in overcoming implementation challenges and ensuring overall acceptance.17,48,72  Beyond pathologists, surgeons are often the direct requesters of telepathology diagnoses and need to actively solicit telepathology and be convinced of its usefulness and reliability. Finally, technicians in charge of slide preparation and scanning are key telepathology users.48  Overall, surgeons' and laboratory technicians' views and reactions towards telepathology deserve more attention in future work.

Referring clinicians are asked to use telepathology to make complex clinical decisions, and they need to trust not only the technology but also the other stakeholders involved in the process. First and foremost, clinicians need to trust the images and telepathology-based diagnosis. Pathologists can be reluctant to base a diagnosis on images sent by another pathologist, technicians need to trust distant pathologists to guide them through the digitization process, and surgeons mistrust the diagnosis of a pathologist they may not be familiar with.73  To create trust, face-to-face introductions of pathologists, capping the number of health care entities a single pathologist interacts with, and, more generally, defining roles clearly can help.20,69,74  Conversely, the introduction of telepathology can have a positive effect on interpersonal trust and generate a sense of collegiality among professionals from the connected sites.22  Trust also involves questions of confidentiality, security, and privacy.75

Although pathologists in general find telepathology acceptable to perform various pathology duties, attitudes towards telemedicine are polarized.76,77  This has been explained by fear that telepathology “could turn pathology services into a geographical unbounded community”55  and by the significant changes in work practice involved.52  Further, some might consider that separating patients and pathology will not allow good clinical work because high-quality pathology can only be performed when there are tight connections with clinicians directly attending the patient. In such cases, pathologists may accept telepathology for local use only, even in nonteaching hospitals. To alleviate these concerns, researchers have suggested focusing on user needs. This can be achieved by addressing the 3 critical challenges of usability, training, and support. Each of these is briefly discussed below.

First, telepathology can be time consuming, a widely investigated usability issue.19,52,53,78  Although the long-term potential to enable time savings has been mentioned, in most cases telepathology slows workflows by adding steps to the pathology process. It requires logging into a patient file, scanning slides, uploading and downloading virtual slides, and navigating through a not always ergonomic application, as opposed to simply picking a slide, positioning it in a microscope, and focusing on the area of interest in a matter of seconds.52  Although the introduction of digital radiology has been shown to improve the productivity of radiologists,60,79  the use of telepathology has the opposite effect for pathologists, which may partly account for telepathology's slower diffusion.

Second, telepathology changes the way pathologists, technicians, and surgeons work and interact. Familiarity with the system and training reduce resistance and improve efficiency.39,52,72,80  Training has also been shown to improve interpersonal communication in virtual teams.81  The learning is not only about technology, but more importantly about adapting oneself to the new work practices involved: surgeons to leveraging the immediate availability of pathology, and pathologists to cooperating with distant colleagues.32  Surgeons and technicians also need to be trained to take over some pathologists' roles in referring sites, and the technicians' training curriculum requires specific adjustments to telepathology activities.82  More research must be conducted on the nature and effectiveness of the training strategies in use.

Third, technical support helps ensure that clinicians and technicians who are less familiar with IT are not discouraged or stopped by technologic hurdles. Support is mainly provided at 2 levels. Internally, targeted users need to have access to qualified people to troubleshoot problems and ensure the system is operational and reliable whenever needed.39  Externally, health care organizations need to partner with reliable IT providers to support and update the systems in use and to tailor the technologic solutions to their particular needs.83  We suggest that more studies be devoted to provide a better understanding of the role mediating institutions such as consulting firms and technology integrators play in helping health care organizations overcome technologic knowledge barriers when implementing telepathology.17

##### Organizational Barriers

Health care organizations also face important challenges such as financing, workflow reengineering, and diagnosis accountability assignment. Each of these challenges will be discussed in turn. First, financing involves 2 distinct challenges: funding upfront investments and, possibly more difficult, funding operational expenses.71  Each stakeholder needs to be properly compensated, be it in a single payer health care system or a private insurance system.17,83  The issue may be less complex in single-location projects and one-to-one networks. In centralized and decentralized telepathology networks, investments are spread over several institutions, the issue of sharing running costs and rewarding each stakeholder becomes more complex, and divergence of interests becomes more likely.84  The sources of financing remain unclear, as researchers call for governments, pathologists, or corporate sponsors to step in and finance running costs.26,37,85  Further research needs to investigate viable financing models for various forms of telepathology projects in both public and private health care systems.

Second, the introduction of telepathology often involves the revision of existing workflows and processes.17,32,44,86  A telepathology system is both a content management tool and a collaborative platform connecting nonexperts (referring clinicians) to experts (pathologists or subspecialty pathologists).74  As a content management tool supporting pathology processes and information, the system is increasingly embedded in existing clinical information systems and their workflows, such as laboratory information systems and electronic medical records.7  This involves interoperability issues requiring considerable integration efforts and harmonization of information and communication standards.3,7,87  When the system is used as a collaboration tool, pathologists need features such as working drafts and prioritization, as well as efficient case assignment. In that regard, 3 distinct models of case assignment are suggested.88  First, in the subspecialty model, subspecialist pathologists directly sign out centralized cases. This is considered an appropriate model for large and centralized institutions with sufficient staffing of subspecialty experts, like the Armed Forces Institute of Pathology.24  Second, in the case triage model, a pathologist assesses the case and, if need be, routes it to a subspecialty pathologist. This prescreening reduces the need for subspecialty pathologists,88  and as a single pathologist is needed, it is adequate for one-to-one or small centralized networks. In a variant of this model, case triage can be tiered, as in the national Croatian telepathology system, where smaller institutions refer their cases to 3 regional centers, which can themselves route their cases to a national center.38  Last, in the virtual group practice model, cases are assigned automatically on the basis of pathologists' characteristics, such as availability or relevant experience. This model is mainly used to provide specialty pathology services to underserved organizations and is likely to be more appropriate for decentralized networks.32,89

Third, telepathology raises accountability issues relating to information privacy, contractual arrangements with other organizations involved, and the extent of coverage provided. One salient issue is whether the consulting pathologist is accountable for the diagnosis.74  In expert groups, consulting pathologists commit to diagnoses, an arrangement appropriate for more structured networks such as centralized or one-to-one networks, where the institutions are integrated and able to set up the conditions for accountability transfer across sites. Expert groups can further be structured around expertise centers, where pathologists have a rotation duty plan that ensures continuity of service.41,86,90  Alternatively, in discussion groups, consulting pathologists leave the final interpretation and diagnostic accountability to the referring clinician and do not necessarily reach a conclusive diagnosis. Discussion groups seem more relevant for decentralized networks such as the iPath project.35  In this interorganizational project, consulting pathologists and referring clinicians from unrelated organizations all over the world freely request and provide consultations.

##### Legal Barriers

Telepathology also raises a series of legal issues and challenges significant enough that as much as “58% [of pathologists] felt that the medicolegal implications of duty of care were a barrier to [telepathology] use.” 72  Further, “telepathology, as seen by the lawyer, is characterized by a geographical distance between the tissue or specimen to be evaluated and the pathologist himself.” 91  This raises the question of which regulations to apply between the consulting and referring sites. Constituencies with an interest in telepathology, such as rural regions with underserved populations, have more advanced laws, whereas other places are lagging behind.92  Another essential legal challenge is related to remuneration, as current regulations do not always allow telepathology reimbursement.20,93  Other legal issues include licensing requirements, data protection and privacy laws, and consent rules.20,33,91  Although several researchers have described and commented on various telepathology rules and regulations,43,51,52,57,91,92  we recommend a recent status update on this important topic.

## COMMENT

This review reveals that managerial issues associated with the acquisition and use of telepathology in health care organizations are multifaceted and multilevel. It also highlights the diversity of telepathology initiatives and contexts and the importance of considering these distinctions when interpreting empirical findings. As shown in Table 3, various network structures are associated with different benefits. The nature and scope of the implementation challenges also seem to evolve and increase with the complexity of the underlying networks.

Table 3.

Key Impacts and Challenges by Telepathology Network Structure

In terms of telepathology impacts, in single-location projects, the dominant rationale is financial, with telepathology being considered as an equal-quality substitute to more costly solutions such as having a resident or roaming pathologist. Larger centralized and decentralized networks, on the other hand, are targeting a more diverse set of benefits, including extending access to pathology to a whole region, achieving substantial economies of scale in workforce and equipment, and improving quality by standardizing care. Conclusive empirical evidence remains to be gathered about these preliminary findings and, more generally, about the role of context in telepathology projects. As shown earlier, comprehensive and rigorous evaluation studies remain rare as of today. As potential benefits are a key motivator leading to individual and organizational adoption, rigorously evaluating their nature and extent represents an important endeavor for future research.

In terms of challenges, in smaller telepathology networks, organizational concerns are less prominent, and implementers are more focused on usability issues. As the project scope widens, organizational issues such as workflows, accountability, and business models gain prominence, as well as organizational structures set up to support end users and the project teams. This echoes the layered model for telemedicine implementation of Broens et al,71  with an implementation focus gradually widening from technology issues to user acceptance, to organizational concerns, to societal issues as the technology matures and the project stage moves from prototype to pilot, to full deployment, and to the professional norm.

To move forward, managerial telepathology research needs to distance itself from anecdotal evidence and descriptive accounts, to leverage existing theories, and to investigate a series of unanswered questions pertaining to telepathology implementation challenges and impacts. More rigorous evaluative studies should be conducted to provide solid evidence of individual and organizational outcomes associated with the deployment of various telepathology configurations and networks. In terms of accessibility to care services, for instance, future studies should quantify the cases where telepathology provides care otherwise unavailable to patients. They should do this by assessing the variations in terms of the number of surgical procedures cancelled, the number of medical complications or surgical procedures performed in 2 stages owing to the absence of pathologists, and the extent to which telepathology actually substitutes for a local pathologist.15  Future studies may address the question of the conditions under which telepathology is recommended versus alternatives such as couriers and in-house pathologists, and what type of benefits to pursue under these conditions. Research comparing multiple telepathology settings and networks will also help refine under which conditions (network structure, distance to the nearest pathologist, medical conditions treated, or level of activity) telepathology is most beneficial.

Moreover, between the individual and organizational levels, telepathology is also the endeavor of a group of people: pathologists, surgeons, and laboratory technicians. Success implies close collaboration and coordination among those health care professionals. We propose several frameworks that could serve as potential conceptual lenses for studying that group dynamic. For a geographically distant group, telepathology could be investigated as a particular form of virtual teams. The multiple dimensions of virtual team configurations such as those proposed by Dubé and Paré94  might allow for a deeper understanding of this form of work arrangements in the health care sector. Another promising research avenue is related to the notion of mutual trust, which has also been extensively investigated in prior research on virtual teams.95  As explained earlier, the role of mutual trust among pathologists, surgeons, and technicians during intraoperative telepathology exams, for instance, becomes even more central.

Another take at addressing group dynamics would be by adopting a socio-technical lens or framework, as suggested by Orlikowski and Iacono.96  It would definitely help in understanding several of the challenges associated with telepathology implementation, such as the emergent changes in technology, workflows, roles, and accountability.97  We posit the more complex forms of telepathology networks represent appropriate settings for investigating these topics more deeply. Finally, given the idiosyncratic nature of telepathology projects dynamics, we argue that the concept of mindful organizing could also contribute to a deeper understanding of how health care professionals collectively enforce an environment conducive to patient safety in a context of uncertainty and complexity reinforced by telepathology.98

To conclude, this review article provides a clear indication of the size and nature of the available knowledge about the impacts and implementation challenges associated with the deployment of telepathology in health care organizations. It reveals that various telepathology network structures exist and, hence, conclusions and recommendations should not be generalized across all initiatives. We encourage researchers to adopt a multidimensional view of telepathology projects in order to compare empirical findings, accumulate knowledge, and, ultimately, provide practitioners with useful guidelines and recommendations.

## References

1
American Telemedicine Association
.
Clinical guidelines for telepathology
. .
2
BCC Research
.
Global markets for telemedicine technologies
. .
3
Garcia Rojo
M
,
Punys
V
,
Slodkowska
J
,
T
,
Daniel
C
,
Blobel
B.
Digital pathology in Europe: coordinating patient care and research efforts
.
Stud Health Technol Inform
.
2009
;
150
:
997
1001
.
4
Park
S
,
Pantanowitz
L
,
Parwani
AV.
Digital imaging in pathology
.
Clin Lab Med
.
2012
;
32
(
4
):
557
584
.
5
Grigsby
J
,
Schlenker
RE
,
Kaehny
MM
,
Shaughnessy
PW
,
Sandberg
EJ.
Analytic framework for evaluation of telemedicine
.
Telemed J
.
1995
;
1
(
1
):
31
39
.
6
Evans
AJ
,
Chetty
R
,
Clarke
BA
,
et al
.
Primary frozen section diagnosis by robotic microscopy and virtual slide telepathology: the University Health Network experience
.
Semin Diagn Pathol
.
2009
;
26
(
4
):
165
176
.
7
Kayser
K.
Introduction of virtual microscopy in routine surgical pathology—a hypothesis and personal view from Europe
.
Diagn Pathol
.
2012
;
7
:
48
.
8
Weinstein
RS
,
Descour
MR
,
Liang
C
,
et al
.
Telepathology overview: from concept to implementation
.
Hum Pathol
.
2001
;
32
(
12
):
1283
1299
.
9
Mieritz
L.
Survey shows why projects fail
.
Gartner Web site
. .
10
Furness
PN
,
Bamford
WM.
Telepathology
.
Curr Diagn Pathol
.
2001
;
7
(
4
):
281
291
.
11
Arksey
H
,
O'Malley
L.
Scoping studies: towards a methodological framework
.
Int J Soc Res Method
.
2005
;
8
(
1
):
19
32
.
12
Levac
D
,
Colquhoun
H
,
O'Brien
KK.
.
Implement Sci
.
2010
;
5
(
1
):
69
.
13
Davis
K
,
Drey
N
,
Gould
D.
What are scoping studies?: a review of the nursing literature
.
Int J Nurs Stud
.
2009
;
46
(
10
):
1386
1400
.
14
Ritchie
J
,
Spencer
L.
Qualitative data analysis for applied policy research
.
In
:
Huberman
AM
,
Miles
MB
,
eds
.
The Qualitative Researcher's Companion
.
Thousand Oaks, CA
:
Sage;
2002
:
305
329
.
15
Trudel
M-C
,
Paré
G
,
Têtu
B
,
Sicotte
C.
The effects of a regional telepathology project: a study protocol
.
BMC Health Serv Res
.
2012
;
12
(
64
):
1
11
.
16
Djamasbi
S
,
Fruhling
AL
,
Loiacono
ET.
The Influence of affect, attitude and usefulness in the acceptance of telemedicine systems
.
J Inf Technol Theory Appl
.
2009
;
10
(
1
):
41
58
.
17
Tanriverdi
H
,
Iacono
CS.
Diffusion of telemedicine: a knowledge barrier perspective
.
Telemed J
.
1999
;
5
(
3
):
223
244
.
18
Szymas
J
,
Lundin
M.
Five years of experience teaching pathology to dental students using the WebMicroscope
.
Diagn Pathol
.
2011
;
6
(
suppl 1
):
S13
.
19
Ho
J
,
Parwani
AV
,
Jukic
DM
,
Yagi
Y
,
Anthony
L
,
Gilbertson
JR.
Use of whole slide imaging in surgical pathology quality assurance: design and pilot validation studies
.
Hum Pathol
.
2006
;
37
(
3
):
322
331
.
20
Wiley
CA
,
Murdoch
G
,
Parwani
A
,
et al
.
Interinstitutional and interstate teleneuropathology
.
J Pathol Inform
.
2011
;
2
:
21
.
21
Graham
AR
,
Bhattacharyya
AK
,
Scott
KM
,
et al
.
Virtual slide telepathology for an academic teaching hospital surgical pathology quality assurance program
.
Hum Pathol
.
2009
;
40
(
8
):
1129
1136
.
22
Almagro
UA
,
Dunn
BE
,
Choi
H
,
Recla
DL.
Telepathology
.
Am J Surg Pathol
.
1998
;
22
(
9
):
1161
1163
.
23
Moser
PL
,
S
,
Heinzle
G
,
et al
.
A cost comparison of telepathology and a visiting pathologist service
.
J Telemed Telecare
.
2003
;
9
(
4
):
200
203
.
24
Dunn
BE
,
Choi
H
,
Almagro
UA
,
Recla
DL.
Combined robotic and nonrobotic telepathology as an integral service component of a geographically dispersed laboratory network
.
Hum Pathol
.
2001
;
32
(
12
):
1300
1303
.
25
Elford
DR.
Telemedicine in northern Norway
.
J Telemed Telecare
.
1997
;
3
(
1
):
1
22
.
26
Nakajima
I.
Forecast on the application of Japanese universal service fund to remote diagnosis for frozen section
.
J Med Syst
.
2010
;
34
(
6
):
1023
1031
.
27
Bashshur
RL.
Telemedicine effects: cost, quality, and access
.
J Med Syst
.
1995
;
19
(
2
):
81
91
.
28
Moser
PL
,
Hauffe
H
,
Lorenz
IH
,
et al
.
Publication output in telemedicine during the period January 1964 to July 2003
.
J Telemed Telecare
.
2004
;
10
(
2
):
72
77
.
29
Nordrum
I
,
Engum
B
,
Rinde
E
,
et al
.
Remote frozen section service: a telepathology project in northern Norway
.
Hum Pathol
.
1991
;
22
(
6
):
514
518
.
30
Kayser
K.
Telepathology in Europe: its practical use
.
Arch Anat Cytol Pathol
.
1995
;
43
(
4
):
196
199
.
31
Swett
HA
,
L
,
Leffell
D
,
et al
.
Telemedicine: delivering medical expertise across the state and around the world
.
Conn Med
.
1995
;
59
(
10
):
593
602
.
32
Têtu
B
,
Fortin
J-P
,
Gagnon
M-P
,
Louahlia
S.
The challenges of implementing a “patient-oriented” telepathology network; the Eastern Québec telepathology project experience
.
Anal Cell Pathol (Amst)
.
2012
;
35
(
1
):
11
18
.
33
Ranson
D.
Telemedicine and the law
.
J Law Med
.
2007
;
15
(
3
):
356
359
.
34
Weinstein
RS
,
Graham
AR
,
Lian
F
,
et al
.
Reconciliation of diverse telepathology system designs: historic issues and implications for emerging markets and new applications
.
APMIS
.
2012
;
120
(
4
):
256
275
.
35
Brauchli
K
,
O'Mahony
D
,
Banach
L
,
Oberholzer M. iPath—a telemedicine platform to support health providers in low resource settings
.
Stud Health Technol Inform
.
2005
;
114
:
11
17
.
36
Hitchcock
CL.
The future of telepathology for the developing world
.
Arch Pathol Lab Med
.
2011
;
135
(
2
):
211
214
.
37
Shiferaw
F
,
Zolfo
M.
The role of information communication technology (ICT) towards universal health coverage: the first steps of a telemedicine project in Ethiopia
.
Glob Health Action
.
2012
;
5
:
1
8
.
38
Danilović
Z
,
Dzubur
A
,
Seiwerth
S.
Concept of telepathology in Croatia
.
Arch Anat Cytol Pathol
.
1995
;
43
(
4
):
282
284
.
39
Horbinski
C
,
Hamilton
RL.
Application of telepathology for neuropathologic intraoperative consultations
.
Brain Pathol
.
2009
;
19
(
2
):
317
322
.
40
Têtu
B
,
Boulanger
J
,
Houde
C.
Telepathology project on virtual slides of eastern Quebec: a clinical project carried out in 21 areas
.
Ann Pathol
.
2010
;
30
(5)(suppl 1)
:
25
27
.
41
Dietel
M
,
Nguyen-Dobinsky
TN
,
Hufnagl
P.
The UICC Telepathology Consultation Center: a global approach to improving consultation for pathologists in cancer diagnosis
.
Cancer
.
2000
;
89
(
1
):
187
191
.
42
Dervan
PA
,
Wootton
R.
Diagnostic telepathology
.
Histopathology
.
1998
;
32
(
3
):
195
198
.
43
Isse
K
,
Lesniak
A
,
Grama
K
,
Roysam
B
,
Minervini
MI
,
Demetris
AJ.
Digital transplantation pathology: combining whole slide imaging, multiplex staining and automated image analysis
.
Am J Transplant
.
2012
;
12
(
1
):
27
37
.
44
Kayser
K
,
Borkenfeld
S
,
Kayser
G.
How to introduce virtual microscopy (VM) in routine diagnostic pathology: constraints, ideas, and solutions
.
Anal Cell Pathol (Amst)
.
2012
;
35
(
1
):
3
10
.
45
Hassell
LA
,
Fung
K-M
,
Chaser
B.
Digital slides and ACGME resident competencies in anatomic pathology: an altered paradigm for acquisition and assessment
.
J Pathol Inform
.
2011
;
2
:
27
.
46
McLemore
EC
,
RT
,
DK
,
Williams
JW
,
Bailey
DP.
Telepathy: maximizing resident exposure to surgical pathology decision making
.
Am J Surg
.
2006
;
191
(
4
):
538
541
.
47
Sohani
AR
,
Sohani
MA.
Static digital telepathology: a model for diagnostic and educational support to pathologists in the developing world
.
Anal Cell Pathol (Amst)
.
2012
;
35
(
1
):
25
30
.
48
Cross
SS
,
Dennis
T
,
Start
RD.
Telepathology: current status and future prospects in diagnostic histopathology
.
Histopathology
.
2002
;
41
(
2
):
91
109
.
49
E
,
Yagi
Y.
Virtual microscopy beyond the pyramids, applications of WSI in Cairo University for E-education & telepathology
.
Anal Cell Pathol (Amst)
.
2012
;
35
(
2
):
93
95
.
50
Bloodgood
RA.
Active learning: a small group histology laboratory exercise in a whole class setting utilizing virtual slides and peer education
.
Anat Sci Educ
.
2012
;
5
(
6
):
367
373
.
51
Pantanowitz
L
,
Valenstein
PN
,
Evans
AJ
,
et al
.
Review of the current state of whole slide imaging in pathology
.
J Pathol Inform
.
2011
;
2
(
36
).
52
Williams
S
,
Henricks
WH
,
Becich
MJ
,
Toscano
M
,
Carter
AB.
Telepathology for patient care: what am I getting myself into?
.
2010
;
17
(
2
):
130
149
.
53
Callas
PW
,
McGowan
JJ
,
Leslie
KO.
Provider attitudes toward a rural telepathology program
.
Telemed J E Health
.
1996
;
2
(
4
):
319
329
.
54
Drummond
MF
,
Sculpher
MJ
,
Torrance
GW
,
O'Brien
BJ
,
Stoddart
GL.
Methods for the Economic Evaluation of Health Care Programmes
.
New York, NY
:
Oxford University Press USA;
2005
.
55
Cornish
TC
,
Swapp
RE
,
Kaplan
KJ.
Whole-slide imaging: routine pathologic diagnosis
.
.
2012
;
19
(
3
):
152
159
.
56
Isaacs
M
,
Lennerz
JK
,
Yates
S
,
Clermont
W
,
Rossi
J
,
Pfeifer
JD.
Implementation of whole slide imaging in surgical pathology: a value added approach
.
J Pathol Inform
.
2011
;
2
(
39
).
57
Kldiashvili
E.
Telemedicine for pathology
.
Stud Health Technol Inform
.
2008
;
131
:
227
243
.
58
Leong
AS-Y
,
Leong
FJW-M.
Strategies for laboratory cost containment and for pathologist shortage: centralised pathology laboratories with microwave-stimulated histoprocessing and telepathology
.
Pathology
.
2005
;
37
(
1
):
5
9
.
59
Harris
T
,
Leaven
T
,
Heidger
P
,
Kreiter
C
,
Duncan
J
,
Dick
F.
Comparison of a virtual microscope laboratory to a regular microscope laboratory for teaching histology
.
Anat Rec
.
2001
;
265
(
1
):
10
14
.
60
Montalto
MC.
Pathology RE-imagined: the history of digital radiology and the future of anatomic pathology
.
Arch Pathol Lab Med
.
2008
;
132
(
5
):
764
765
.
61
Agha
Z
,
Weinstein
RS
,
Dunn
BE.
Cost minimization analysis of telepathology
.
Am J Clin Pathol
.
1999
;
112
(
4
):
470
478
.
62
Becker
RL
,
Specht
CS
,
Jones
R
,
Rueda-Pedraza
ME
,
O'Leary
TJ.
Use of remote video microscopy (telepathology) as an adjunct to neurosurgical frozen section consultation
.
Hum Pathol
.
1993
;
24
(
8
):
909
911
.
63
Loane
MA
,
Bloomer
SE
,
Corbett
R
,
et al
.
Patient cost-benefit analysis of teledermatology measured in a randomized control trial
.
J Telemed Telecare
.
1999
;
5
(
suppl 1
):
1
3
.
64
Dunn
BE
,
Choi
H
,
Almagro
UA
,
Recla
DL
,
Davis
CW.
Telepathology networking in VISN-12 of the Veterans Health Administration
.
Telemed J E Health
.
2000
;
6
(
3
):
349
354
.
65
Wilbur
DC.
Digital cytology: current state of the art and prospects for the future
.
Acta Cytol
.
2011
;
55
(
3
):
227
238
.
66
Eide
TJ
,
Nordrum
I.
Current status of telepathology
.
APMIS
.
1994
;
102
(
12
):
881
890
.
67
Shanmugaratnam
K.
Happenings in histopathology—a post-World War II perspective
.
.
2007
;
36
(
8
):
691
697
.
68
O'Malley
DP.
Practical applications of telepathology using morphology-based anatomic pathology
.
Arch Pathol Lab Med
.
2008
;
132
(
5
):
743
744
.
69
Carter
AB.
Stepping across borders into the future of telepathology
.
J Pathol Inform
.
2011
;
2
:
24
25
.
70
Attewell
P.
Technology diffusion and organizational learning: the case of business computing
.
Organ Sci
.
1992
;
3
(
1
):
1
19
.
71
Broens
THF
,
Huis in't Veld RMHA, Vollenbroek-Hutten MMR, Hermens HJ, van Halteren AT, Nieuwenhuis LJM. Determinants of successful telemedicine implementations: a literature study
.
J Telemed Telecare
.
2007
;
13
(
6
):
303
309
.
72
Dennis
T
,
Start
RD
,
Cross
SS.
The use of digital imaging, video conferencing, and telepathology in histopathology: a national survey
.
J Clin Pathol
.
2005
;
58
(
3
):
254
258
.
73
Baruah
MK.
The practice of telepathology in India
.
.
2005
;
51
(
4
):
316
318
.
74
Brauchli
K
,
Oberli
H
,
Hurwitz
N
,
et al
.
Diagnostic telepathology: long-term experience of a single institution
.
Virchows Arch
.
2004
;
444
(
5
):
403
409
.
75
Blobel
B.
Security and privacy services in pathology for enabling trustworthy personal health
.
Stud Health Technol Inform
.
2012
;
179
:
203
217
.
76
Stanberry
B.
Telemedicine: barriers and opportunities in the 21st century
.
J Intern Med
.
2000
;
247
(
6
):
615
628
.
77
Gabril
MY
,
Yousef
GM.
Informatics for practicing anatomical pathologists: marking a new era in pathology practice
.
Mod Pathol
.
2010
;
23
(
3
):
349
358
.
78
McClintock
DS
,
Lee
RE
,
Gilbertson
JR.
Using computerized workflow simulations to assess the feasibility of whole slide imaging full adoption in a high-volume histology laboratory
.
Anal Cell Pathol (Amst)
.
2012
;
35
(
1
):
57
64
.
79
Nitrosi
A
,
Borasi
G
,
Nicoli
F
,
et al
.
A filmless radiology department in a full digital regional hospital: quantitative evaluation of the increased quality and efficiency
.
J Digit Imaging
.
2007
;
20
(
2
):
140
148
.
80
Bamford
WM
,
Rogers
N
,
Kassam
M
,
Rashbass
J
,
Furness
PN.
The development and evaluation of the UK national telepathology network
.
Histopathology
.
2003
;
42
(
2
):
110
119
.
81
Warkentin
M
,
Beranek
PM.
Training to improve virtual team communication
.
Inform Syst J
.
1999
;
9
(
4
):
271
289
.
82
Giansanti
D
,
Castrichella
L
,
Giovagnoli
MR.
Telepathology requires specific training for the technician in the biomedical laboratory
.
Telemed J E Health
.
2008
;
14
(
8
):
801
807
.
83
Hasegawa
T
,
Murase
S.
Distribution of telemedicine in Japan
.
Telemed J E Health
.
2007
;
13
(
6
):
695
702
.
84
Pagni
F
,
Bono
F
,
Di Bella
C
,
Faravelli
A
,
Cappellini
A.
Virtual surgical pathology in underdeveloped countries: the Zambia project
.
Arch Pathol Lab Med
.
2011
;
135
(
2
):
215
219
.
85
Hipp
JD
,
Sica
J
,
McKenna
B
,
et al
.
The need for the pathology community to sponsor a whole slide imaging repository with technical guidance from the pathology informatics community
.
J Pathol Inform
.
2011
;
2
(
31
).
86
Aas
IH.
Telemedical work and cooperation
.
J Telemed Telecare
.
2001
;
7
(
4
):
212
218
.
87
Daniel
C
,
Booker
D
,
Beckwith
B
,
et al
.
Standards and specifications in pathology: image management, report management and terminology
.
Stud Health Technol Inform
.
2012
;
179
:
105
122
.
88
Bhattacharyya
AK
,
Davis
JR
,
Halliday
BE
,
et al
.
Case triage model for the practice of telepathology
.
Telemed J E Health
.
1995
;
1
(
1
):
9
17
.
89
Kayser
K
,
Kayser
G
,
D
,
Oehmann
A.
New developments in digital pathology: from telepathology to virtual pathology laboratory
.
Stud Health Technol Inform
.
2004
;
105
:
61
69
.
90
Brauchli
K
,
Oberholzer
M.
The iPath telemedicine platform
.
J Telemed Telecare
.
2005
;
11
(
suppl 2
):
S3
S7
.
91
Dierks
C.
Legal aspects of telepathology
.
Anal Cell Pathol
.
2000
;
21
(
3–4
):
97
99
.
92
Leung
ST
,
Kaplan
KJ.
Medicolegal aspects of telepathology
.
Hum Pathol
.
2009
;
40
(
8
):
1137
1142
.
93
Weinberg
DS.
How is telepathology being used to improve patient care?
Clin Chem
.
1996
;
42
(
5
):
831
835
.
94
Dubé
L
,
Paré
G.
The multifaceted nature of virtual teams
.
In
:
Pauleen
D
,
ed
.
Virtual Teams: Projects, Protocols and Processes
.
Hershey, PA
:
Idea Group Publishing;
2004
:
1
39
.
95
Jarvenpaa
SL
,
Leidner
DE.
Communication and trust in global virtual teams
.
Organ Sci
.
1999
;
3
(
4
):
791
815
.
96
Orlikowski
WJ
,
Iacono
CS.
Research commentary: desperately seeking the “IT” in IT research—a call to theorizing the IT artifact
.
Inform Syst Res
.
2001
;
12
(
2
):
121
134
.
97
Davidson
EJ
,
Chismar
WG.
The interaction of institutionally triggered and technology-triggered social structure change: an investigation of computerized physician order entry
.
MIS Q
.
2007
;
31
(
4
):
739
758
.
98
Trudel
MC
,
Paré
G
,
Laflamme
J.
Health information technology success and the art of being mindful: preliminary insights from a comparative case study analysis
.
Health Care Manage Rev
.
2012
;
37
(
1
):
31
42
.

## Author notes

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