key: cord-0907822-8i2fbq92
authors: Chiou, Paul
title: Learning Cytology in times of pandemic: an educational institutional experience with remote teaching
date: 2020-06-10
journal: J Am Soc Cytopathol
DOI: 10.1016/j.jasc.2020.05.004
sha: 62883478c551c78ac80811fb56a46826eb17776c
doc_id: 907822
cord_uid: 8i2fbq92

Abstracts Introduction As the coronavirus pandemic swept across national and state borders, institutions of higher learning, including cytology, began closing campuses and moving instructions on-line. We described a method of remotely teaching cytology in our institution, which includes utilizing the tele-cytology concept used in Rapid Onsite Evaluations (ROSE) and using remote conferencing/educational tools to conduct eCytology learning. This is a cost-effective way to transition a traditional in-classroom program into online teaching in cytology. It can also be implemented quickly. Methods In March 2020, our cytology program developed a method for teaching cytology remotely. The distance-learning teaching method included the use of remote conferencing (Zoom) and learning management platforms (Canvas) to present lectures and administer tests. Remote multi-head sessions were conducted by adapting the tele-cytology ROSE concept which attach a mobile device to the microscope to transmit live video to remote learners. Results When asked about their experiences with online learning, students responded positively to their experiences. All students indicate a willingness to attend classes remotely in the future, even when the traditional in-classroom learning option is available. Conclusion We present a method for educating students remotely through the use of existing technology that is affordable and could be implemented quickly by nearly all cytology education programs.

As the coronavirus pandemic spread across national and state boarders, governors and health officials began instituting stricter rules to flatten the curve of the spread and to reduce the incidence of new COVID19 cases. Non-essential business entities, including colleges and universities, began closing its physical campuses and moving instructions online (1). The coronavirus disease 2019 (COVID-19) is a pandemic with the SAR-CoV-2 virus, named for the spikes that protrude from their surfaces, resembling sun's crown (2, 3) . In the past, there was the H1N1 "Spanish" influenza pandemic responsible for 50 million deaths globally and infected as much as a third of the world population over a long period of time (3) (4) (5) . Currently, both the magnitude and duration of the viral impact on global economy remains mostly unknown, there is a growing speculation that limited "sheltered-in-place" will remained in effect and remote learning for students will be the new normal. It is, therefore, important to address best practices in remote cytology learning and pathology education. While the field of cytology has seen many technological advances in recent years, including tele-cytology and Whole Slide Imaging (WSI), there has been a dearth of best practice literature on remote teaching in the profession in the United States. Furthermore, even less schools have move entirely online, making this sudden transition challenging for most cytology training institutions.

The larger pathology sector has benefited from the recent increase in computing processing power, storage capability, as well as broadband speed. A decade ago, digital cytology refers to the use of cameras to acquire static images but it means so much more today. Digital cytology has shifted from static images toward whole slide imaging (WSI), which involves scanning a glass slide at various magnifications to form a digital slide. The evaluation of the digital slide is done, not on a microscope, but on a large computer monitor or tablet computer with a mouse or stylus. The advancement in the field in recent years has enormous positive impacts, including interactive virtual continuing education, electronic proficiency testing, and the development of artificial intelligence tools for greater pathology laboratories (6, 7) .

The progress in the digitalization of cytology specimen has been more challenging than biopsy or histology samples due to technical difficulties. In essence, histopathology specimens are easier because they are relatively flat and can be capture digitally via single plane digital scanner. Cytology preparations, on the other hand, are more problematic due to the intrinsically three-dimensional nature and the special technical requirements needed, to produce digital renditions of the specimen (8) . Other barriers to adoption in digital cytology include steep learning curve, regulatory hurdles, cost of initial adoption, bottlenecks, lack of common standards, and the complicated return on investment calculations (9) .

Tele-cytology or the remote transmission of real-time cytology video, is a very different application than WSI. Instead of a digital recreation of the entire slide, tele-cytology is simply the sharing of what is seen under the microscope in real time. This technology was problematic in its earlier days due to the slow internet connectivity and the limited usage of small mobile devices. Today, problems with image quality and transmission have largely been resolved, thanks to the technological advancement in internet bandwidth, the increased in the prevalence of sophisticated mobile devices, and the availability of realtime mobile communication apps (10) (11) (12) . This approach is becoming more commonly utilized in the performance of the fine needle aspiration adequacy assessments and there appears to be a growing interest in the laboratory community for cytotechnologists that are proficient in tele-cytology and ROSE (13, 14) .

Despite the advancement in the imaging technology, there are only three cytotechnology programs that currently use virtual microcopy in limited capacity, because WSI can be an expensive proposition for many of the programs and laboratories. Many cytology schools and laboratories are not interested in digital cytology and do not consider these skill-sets to be important because of the upfront investments involved in the implementation and set-up (13) . In one recent survey, when schools were asked why they have not embrace virtual microscopy (VM), they mentioned cost as a major reason for the nonadoption (15) . Additionally, the scanning and conversion of glass slides into digital VM image is a resource intensive and time consuming process, requiring manpower, which many schools on tight budget simply do not have. Herein, we present our experience with online cytology instructions, that utilizes digital platform similar to tele-cytology to teach remotely. This can be a low cost alternative to digital scanners for online teaching. In our current environment where many campuses remained closed, this cost-effective remote teaching approach in cytology can be implemented quickly. Moreover, our experience can serve as an inexpensive exploratory foray into e-teaching in cytology for many training programs before committing immense resources and funding to the development of a complete digital virtual microscopy library.

The key to our cytotechnology remote teaching experience centered on the use of easy and intuitive video teaching and communication platforms. At our institution, we utilize Zoom conferencing (San Jose, CA) and Canvas (Salt Lake City, UT) as our online and learning management teaching tools for lectures, microscopy sessions and tests.

Lectures -The lectures were prepared using Power Point and shared in real-time through the Zoom platform. In the weeks leading up to the migration to on-line teaching, the faculty attended a Zoom for teaching webinar orientation to learn the basic operations, such as how to record and post the teaching sessions into learning modules for the students who missed class. During our first synchronous online lecture, we explained net-etiquette to the students, including the need to keep their video on at all times during class to encourage engagement and classroom participation. The students were also instructed to dress and behave as if on campus, with professional attire and behavior (i.e.: no pets or friends in the background).

Microscopy -In our remote synchronous microscope sessions, we utilized the low-cost mobile smartphone interface that allows for connection between personal mobile phone with our microscope. The platform we used for our microscope is LabCam ™ (Fig 1 & Fig 2a) . The concept is similar to telecytology in that we attached our smartphone to a microscope head to share live microscope field of views (FOVs) with remote students who were logged in through the Zoom platform. This low cost approach allows the instructor to conduct a multi-head session and share what is seen under the microscope live, up to 300 students at any given time. The remote session was recorded on cloud and can be posted to our learning management platform (Canvas ™) for those that have missed class. Zoom utilizes both front and rear camera on our smartphone so that the teacher can switch the focus from the images under the microscope to face instructors as needed.

Interactive resources -There are also publicly available educational digital cytology websites on the internet that we had shared with the students and had asked them to review as supplemental teaching aides to our lecture images. Some of the interactive cytology websites are commercially available through private vendors like Hologic while others are made possible from cytopathology associations, like the International Academy of Cytology (IAC). These sites provided educational digital slides where the instructors can zoom into areas of interest on a virtual slide by the click of a mouse or scroll-wheel to discuss with the students in real-time. These resources were helpful for students and were used routinely in our remote teaching (Table 1) .

Glass slides -In addition to lectures, synchronous multi-head sessions, and interactive digital cytology resources, we have made study-set glass slides available for students to pick-up. These study slides, normally available in our classroom slide library, were packaged and divided evenly for the students to take. The learners were also each given a loaner microscope and 150 study set slides initially. Add and drop areas for slides were designated on-campus should they require to pick-up additional glass slides.

The students were asked to submit their weekly cytology screening log to the education coordinator to ensure they were making acceptable progress in their screening.

Tests that are heavy in theory were administered through our learning management platform, Canvas, testing the student's knowledge through short answer essays and multiple choice questions. The time allotted was shortened so that there will not be time for students to be reviewing notes while taking the tests. Additionally, the order of the test questions was randomized so that the questions are different for each of the students, minimizing one texting the other for quick answers. In addition to Canvas platform tests, we also have weekly image quizzes where the students were asked to apply diagnostic criteria to the image of the unknown cytology entities appearing on their screens, similar to the American Society for Clinical Pathology's board exams (ASCP BOC). Images and questions relevant to the week's lecture were displayed one at a time through the Zoom platform. In order to preserve the integrity of the exam, the amount of time per question was shortened (compared to in-classroom time allotted per question) and students were asked to private message their answers to instructors directly at the end of each question. At the completion of the test, students were also asked to submit their entire test to the faculty before reviewing them as a class.

Test slides were administered using LabCam ™ and Zoom™, the same way they were utilized in teaching remote microscopy. The faculty shared what was seen under the microscope, in real-time, with the remote learners and asked for their diagnosis. To test the students' locator skills, the instructor screened a given area and asked for a diagnosis. Other question types included the reviewer showing a few dotted areas of interest for an interpretation. In order to preserve the integrity of the testing, we have also asked the students to private message (PM), via Zoom platform, the answer after every question. At the end of the slide test, students will compile their responses onto a single document by copying and pasting answers from their PM log to email instructor, before the class reviews the tested slides together (Table 2) .

Throughout the course of the remote teaching, the students were asked regularly, via anonymous polls on Zoom, their reflections regarding the efficacy of the transition. They were asked specifically on their thoughts regarding the remote learning experiences and whether they would consider attending on-line sessions, if given both traditional and distance-learning options in the future.

Prior to the start of each class, informal anonymous polls were generated from Zoom as a way to interact with all of the cytology students as they log into the online classroom platform. Most of the weekly poll questions were on how they were coping with the stressors related to the pandemic. Questions such as frequency of exercise during the week, to the number of virtual interactions with others, were posted and discussed as a way to understand whether the students were coping successfully with the pandemic. Two informal polls, taken during the second and third weeks into the lockdown were related to their experiences with online learning. The students were free to take the poll anytime it was open until the conclusion of the Zoom session at the end of the class. Only the results of the two polls relevant to online learning were recorded (table 3 & 4) .

The students were asked twice on their remote learning experiences relative to in-classroom learnings and they have indicated that the two were comparable. We moved the instructions online during the 9 th week of the semester. The remaining six weeks of instructions, or 40% of the semester hours, were conducted entirely remotely. According to our informal Zoom poll, when the students were asked, "How are you enjoying remote learning", 67% (n=2) of the respondents selected "Excellent, absolutely enjoying it" with 33% (n=1) deciding not to answer (table 3) . When asked, "Would you consider listening to lectures on-line in the future if given the options of both traditional and on-line learning modules?", all of the students responded positively, with 33% (n=1) indicating they'd log in often remotely and 67% (n=2) suggesting they'd do so occasionally (table 4) .

Furthermore, as we compared the results of the students' course evaluations in the Spring semester versus the same course for the Fall, the average score for the "course content & structure" was the same for both semesters at 4.67. It is on a scale of 1 to 5, with 1 being the lowest and 5 the highest rating. "Course content & structure" category measures a student's overall evaluation of the program, asking questions such as whether the course objectives were clearly stated in the syllabus, whether course content delivered met course objectives, or whether lessons were presented in a logical manner.

As tele-medicine becomes more widely accepted, so too has the possibility of educating the cytotechnologists remotely. There are a few tele-cytology articles in the medical literature that showed the efficacy for the use of mobile devices, such as I-phone, for tele-cytology (16) (17) (18) . The Covid19 pandemic has sped up the evolution of our profession to become more digitally savvy as we evaluate creative ways to bring the education to our students in the midst of social-distancing and physical classroom closures. The following five points are reflections from the implementation of our remote learning program, that may be helpful for others that are looking to teach remotely:

1. Slowing down: There is a split millisecond of lagged time for the image to be transmitted live to remote learners, depending on the connection speed. Therefore, the faculty behind the microscope must be cognizant at all times while conducting the synchronous multi-head session, to slow down when moving the stage or after adjusting the magnification. A rule of thumb is to count to two after changing your FOV or when switching objectives from lower to higher magnification or vice versa. 2. Reviewing the Zoom screen often: Users may prefer to use the regular head while placing the LabCam™ on a separate multi-head so it is important to review both often (Fig 2b) . Since what the remote learners are seeing in real-time during microscopy sessions are reflected on the presenter's Zoom screen, the faculty should periodically review the screen to ensure things are centered or the electronic pointer's light intensity is set appropriately. 3. Reducing labor-intensive practices: Since the act of requiring remote students to private message the instructor in Zoom after every question may be labor intensive, a more elegant way would be to explore the option of setting up two cameras, one behind and another in front, so the instructors can see learner's screen and face. Some of the other allied health programs have utilized this model where the school issued iPads were used as the second camera for the students. 4. Coming to campus: Students were sent home with slides to review and asked to come on campus to pick up more as needed. In the future, it is a good idea to explore other ways for delivering slides and practicum tests, including a protocol for packaging and sending slides to students' homes for review, instead of asking them to come on campus. 5. Incorporating active learning activities: Studies have shown that students enjoy interactive activities. Moreover, meta-analysis have shown that active learning activities increase average exam score by 6% and students are 1.5 times less likely to fail (19, 20) . In the future, it is a good idea to incorporate more interactive on-line tools, like Zoom Polling, Poll Everywhere, Kahoot!, that are readily available and easy to incorporate into remote teaching.

While the results of the study are beneficial for cytology teaching programs moving to distance education, there are limitations to the findings. First, is the bias on the part of respondents to please the questioner. Second, the framing of the questions could also create bias and influence the choice of responses as they were not piloted to ensure they would be easily understood. Third, it is a small sample population. Fourth, this is the on-line experience of one cytology institution and may not be directly generalizable or applicable to all geographical regions of the United States.

Future iterations of the online teaching will incorporate many of the practices described above. Our program hopes to collect more information about how other cytology programs are adapting to their new post-pandemic environment. Many colleges and universities across the states have become creative in its content delivery while others struggled with technical issues. As an example, medical students at Cleveland began using augmented reality programs as a substitute for cadavers used in Anatomy classes (21) . As institutions are grappling with whether and how to move from a traditionally in-classroom to remote teaching, our experience can serve as an inexpensive exploratory foray into eteaching in cytology before committing immense resources and funding to develop a complete digital virtual microscopy library. While obtaining a digital scanner may be necessary at the end, the use of LabCam™ or similar devices may be the preferred interim step in the current pandemic environment, where the campuses remained close or with limited restrictions.

Having a strong remote educational platform and an adequate comfort with tele-cytology instructions are essential as the world is becoming increasingly digitalize in the aftermath of the coronavirus pandemic. Laboratories and cytology schools in particular must also evolve to stay relevant. The use of tele-cytology to multi-head takes practice but is easy to learn. The important thing is to slow down to allow for lag and to be watching the broadcast while using your microscope. Method 2: Using existing digitalized cytology websites to share with students. The instructor can share the evaluating process through Zoom.

These commercially available or free pre-digitalized slides are very useful teaching aid for cytology students, as complement for screening. The remote equivalence is comparable to traditional testing but the current process of asking the learners to "PM" answers after each question is labor intensive. 2 Microscope Testing Method 1: Using tele-cytology technology, the instructors screening the areas of interested or reviewing dotted areas for the learners to simulate screening.

The use of "tele-cytology" approach to testing is fine with testing recognition of entities under the microscope but is not great at testing the learners' locator and screening skills. Method 2: Using existing digitalized cytology websites to test students. This method works well if you have own digital scanner to create your own library. Otherwise, it is hard to prevent students from looking up answers. 3 Theory Testing

Using the learning management system, Canvas ™ Comparable to in class experience since questions are randomized so that each students will have a different test than another. 

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