Initial Publication Date: April 10, 2020

Prevalence of Antibiotic Resistance in the Environment (PARE), Tufts University

Carol Bascom-Slack, Tufts University

The PARE CURE studies the prevalence of antibiotic resistant in the environment, couched in the broader "One Health" concept - that human health is related to the environment and animal health. The CURE is modular in nature, with each module requiring roughly three traditional laboratory course periods (of 2-3 hours each). All modules are related to the study of environmental antimicrobial resistance. The PARE network consists of implementing instructors around the country, academic researchers, and industry partners.

The program began with a "core module" in which students use standard microbiological techniques (e.g., serial dilutions, plating, and colony counting) to determine the percent of antibiotic-resistant microbes in a local soil sample. Students record their prevalence data and sample collection site characteristics into a national database with a live interactive map. The CURE has since been expanded to create a library of "extension modules," including a case study (i.e., no wet lab) based on a seminal paper, a known outcome wet lab that introduces students to the context of environmental antimicrobial resistance and molecular techniques used in later modules, and a series of authentic research modules (i.e., unknown outcome). The modular nature allows instructors flexibility to insert authentic research (via the modules) into their classes in ways that are compatible with their course goals and the resource availability. The modules use common, standardized methods, which means that student-generated data can be compared across a broad geographic range.

CURE Development

How did your CURE initiative get started? When I taught semester-long CUREs, I witnessed the student excitement and learning that can result from participation in classroom-based research. However, through conversations with instructors at a range of different institution types, I recognized the need for a different, flexible and easier-to-implement model. Many instructors do not have complete control over their course curriculum or do not feel they have the "bandwidth" to begin their foray into CUREs with a full semester course. I created PARE to be easily disseminated and inserted into an existing course. I piloted the first PARE module by asking a two colleagues if I could try it out in their lab section (one at my own institution and another in another state). They received no compensation for supplies or their time. The pilot implementation went well; students were able to generate data and the cost and time commitment were low. Based on this small proof of concept, I applied for an NSF IUSE grant. It was funded and supported dissemination of the PARE CURE. Currently, we have students at about 120 undergraduate institutions contributing data. The program runs mostly autonomously at each institution but has served as a catalyst for building and sustaining a CURE culture in many cases (see "Indicators of Success" below).

How was the CURE integrated into curricula? Instructors generally start by replacing a few of their current laboratory class periods with the core module. After the opportunity to "test the waters" with classroom research, most instructors decide to expand the research experience for their students within the same course, by extending to more sections or by creating a follow-up, more advanced course. In addition, some student participants continue their PARE-related research outside of the classroom by working in a research lab under the mentorship of the CURE instructor. This affords them a much greater opportunity to make decisions guiding their research and provides more autonomy. Additionally, this has worked particularly well at non-research-intensive undergraduate institutions in which the instructor may not have a research emphasis. In that sense, the program can complement a faculty member's own research or even catalyze a research program for the faculty mentor. PARE is used in courses ranging from non-majors, introductory biology, majors or health science microbiology and environmental biology. The courses in which PARE is integrated are generally always courses that are required and/or pre-existing courses.

How has the CURE shifted over time as the research progresses? We believe a key to our success has been starting with a small project that lends itself to additional research in many directions. This has allowed instructors to take ownership of the project in their classrooms and allows us, at a programmatic level, to continue to offer new opportunities for instructor participants. We are always open to listening to participating instructors for how they have expanded the research experience in their classrooms. We work with these instructors to create new modules using a standard template of instructions for implementation ranging from supplies needed, methods, places where students are likely to struggle, etc.

We don't anticipate that any of the modules will need to change over time, but some may surpass the core module in popularity as research progresses. We will need to generate a LOT of data that is currently crowd-sourced from the student participants, so we don't envision ever reaching saturation. Analysis of the larger dataset is something that students or researchers can do.

What barriers or challenges have you faced in implementing the CURE initiative?

Instructor level: We have surveyed and interviewed our instructors pre- and post-implementation about barriers (perceived and encountered). Surprisingly, PARE instructors did not commonly cite time constraints (either personal time or time in the semester) as a barrier. Similarly, some first-time implementers cited cost as a barrier, but this was also not very common. The largest perceived barrier reported by PARE instructors, prior to implementation, are concerns about student readiness for research and student reluctance.

Programmatic level: The project is relatively easy to administer at the programmatic level, but it does take time. Our main barrier to sustainability has been securing funds for the administrative costs to keep the program running and to add research modules of interest to clinician researchers and the agricultural community. Because the program serves institutions beyond my own, my own institution has not recognized the importance of contributing to administration of PARE and I have not had buy-in from the development office to secure funds from private foundations. Other CUREs have done this successfully, so that is a model we need to push. At the research level, developing and optimizing new modules for student use is not developing new cutting-edge science, but rather optimizing existing techniques. This has precluded us from obtaining funding from agencies that fund innovative research science. We have managed to secure small internal funds to experiment with development of new scientific innovations (new modules). Key to this success has been networking within my institution relentlessly, pitching the program and gaining interest from other researchers.

Another programmatic-level barrier has been curating student-generated "messy" data. This problem is not insurmountable, but requires some external funding to solve this challenge in a comprehensive way. In the meantime, we are managing to perform some time-consuming curation and have integrated some automated curation.

Student level: Post-implementation, PARE instructors do not report major challenges with students. The main challenges reported pre-implementation relate to lack of readiness for research and reluctance to engage. Post-participation, students generally report engagement and interest in the research topic and often report that participation confirmed their intended career path. On a programmatic level, our main student-related challenge has been finding a way to curate the abundance of "messy" data generated (see above).

Indicators of success:

The PARE project has three overarching aims related to instructor, scientific, and student outcomes.

1) For instructors, the goal is to provide a low-barrier pathway to implement research in their classrooms and create a sustained CURE culture within their classroom or their institution.

Our main indicators are success are instructor participation, retention and the success of PARE as a catalyst to introduce and sustain a CURE culture, either within the implementing instructor's classroom or extending beyond their classroom to other colleagues in the department. Over 150 instructors at 125 institutions have implemented PARE and the program is adding about 20 institutions per year without active recruitment or offering any funding to implementing instructors. Participating institutions are roughly equally distributed among associate's/two year colleges, baccalaureate, master's granting and doctoral granting. We believe our low cost, modular approach provides an example of how a culture of CUREs can be established at an institution without external funding at that institution.

For example, at The Ohio State University, the core PARE module was first integrated into one section of introductory biology (by Dr. Jennifer Larson, currently at Capital University); subsequently, it was expanded to include bioinformatics (leading to production of an extension module), and expanded to all laboratory sections (Dr. Lubomira Cubonova). Another semester-long honors laboratory course has been developed that incorporates PARE-related work (Dr. Adam Andrews). Dr. Larson has also worked with undergraduate student researchers outside of the course, in PARE-related independent research. As another example, at Birmingham-Southern College, a PARE instructor (Dr. Kevin Drace) expanded on the core module and used it as a template to develop a semester-long CURE called MARE (Metal and Antibiotic Resistance Evolution); MARE has been piloted as the replacement for the freshman-level introductory biology laboratory. At Adams State University, Dr. Adam Kleinschmit (currently at the University of Dubuque) expanded the experience beyond the core PARE module to include follow-up work that led to generation of an "extension module" that is available to all PARE instructors. In addition, he has worked with students doing independent research (outside of class time) to pilot the methods for new PARE-related modules. These are just a few examples of how PARE has impacted students, instructors and departments.

Overall, we feel that the flexibility of PARE to be adapted to the needs and resources of the institution and instructor and its low cost are the keys to its success as a catalyst for sustained change.

2) For the scientific community, our goal is to create a database of environmental surveillance data to allow identification of antimicrobial resistance "hotspots". This, in turn, could target areas for stewardship efforts.

Our main indicators of success for this effort include the creation of a database with thousands of student-generated data points of antimicrobial surveillance data from locations around the world. Another indicator of success is buy-in from a clinician-researcher who specializes in infectious diseases and antimicrobial infections. Dr. James Kirby (Harvard Medical School) is interested in the student-generated data and is working with us to inform us of the most clinically-relevant markers of resistance. Similarly, we are collaborating with a team from the Tufts School of Engineering (led by Dr. Amy Pickering) to develop and optimize methods for detection of these rare, but clinically important, antimicrobial resistance genes from environmental DNA. Likewise, we have partnered with the miniPCR company to distribute the reagents for this (and other) molecular modules. Tufts has recently created a new Center for Integrated Management of Antimicrobial Resistance, which has recognized the value that this program provides, both from an educational and surveillance perspective. Having that support lends credibility to the program as a source of usable data. These groups are all interested because they believe in the potential of our student-generated surveillance data.

3) For students, our goal is to provide opportunity to engage in a relevant, global research project related to students' local environment.

In self-report surveys, students indicate interest in the project, specifically they like knowing that they are contributing to a national project. Instructors also report that the relevance to students' lives and the collaborative nature of the project is a motivator for them and leads to engagement. Student feedback (using anonymous post-participation surveys) is largely positive and a majority report affirmation of their intended career goals as well as learning about a subject (environmental antimicrobial resistance) for which they were previously unaware.

We have collaborated with a team of PARE instructors to co-develop and pilot a comprehensive student assessment (pre/post) that measures learning related to intended program learning objectives. Dr. Adam Kleinschmit (University of Dubuque) is leading the effort to pilot this among a large group of PARE instructors. Pilot survey results show significant gains pre/post.

Has your CURE resulted in additions to databases that scientists access, scientific publications, or community reports?

Databases: We have a Geographic Informational System-based map and database of environmental antimicrobial prevalence data generated by students around the country. The incoming data are "messy" and require substantial curation (see challenges, above). We have built in some automated curation capability as well as creating different modules that generate data less prone to error. The data are uploaded by students and are viewable immediately.

Publications and Community Reports: We have published the core PARE module and the PARE network of instructors have collectively contributed several peer reviewed posters at meetings. Similarly, undergraduates who have participated in the program have presented their work at symposia. A list of these, as well as PARE-related invited seminar talks can be viewed on our Tufts website.

E.A. Genné-Bacon and C.A. Bascom-Slack. The PARE Project: A Short Course-Based Research Project for National Surveillance of Antibiotic-Resistant Microbes in Environmental Samples. J. Microbiol. Biol. Educ. Oct. 2018 vol. 19 no. 3. doi:10.1128/jmbe.v19i3.1603


How were resources identified and sought early on? As mentioned above, CURE development was enabled through an NSF grant. $650 start up supply money was offered to approximately 10 instructors per year for the first three years of the program. Currently, program assessment indicates that cost is not an obstacle for initiating or continuing use of the program for the majority of institutions who implement. Further, we have been adept at leveraging network instructors in exchange for opportunity to present or co-author publications and grants. PARE network has co-developed new methods, curricular modules, and assessment instruments. Likewise, we have leveraged support from external researchers who have recognized the potential value of the research generated by the students. A clinician-researcher, an engineering professor, and a company have all offered services without funding support.

How were resources sustained over time? The program requires little outside funding for classroom implementation and its low cost allows replacement of old curriculum with a CURE-based curriculum. The modular structure allows an incremental replacement of old curricula a few class periods at a time and we hear from participating instructors that this is important. When we survey instructors, cost or equipment has never been reported as a major concern rendering the program naturally sustainable. Continued funds for program administration, evaluation and database maintenance are helpful to keep the community connected and to allow the program to keep innovating. However, without top-down support, each individual program would thrive. In other words, the program at each institution is relatively autonomous.

Stakeholder Buy-In

How was student buy-in achieved? Usually this CURE is integrated into an existing class so there is no student "buy in" per se. I don't believe many/any students are taking the class because of the CURE aspect.

How was faculty buy-in achieved? The first three years I advertised on list servs and promoted at the American Society of Microbiology Conference of Undergraduate Educators (ASMCUE). I provided $650 in supply funding to incentivize participation, but that seemed not to be a driver (about 50% of faculty claimed the reimbursement). There is currently no recruitment. Faculty approach me via word of mouth; we draw about 20 new instructors/institutions per year. The majority of these faculty have already been seeking knowledge about CUREs and are interested in integrating a CURE into their existing classroom. They often learn about PARE through their knowledge-seeking activities.

The program has naturally disseminated within institutions in four ways:

  1. The duration of the CURE in the implementing classroom has been extended either through individual instructor initiative or through implementation of "extension modules" that we have created—all short term CURE modules related to the original PARE module.
  2. An instructor integrated the CURE into their sections of a multi-section course. Based on the success, instructors who taught other sections adopted in subsequent years.
  3. The success of PARE has prompted departmental discussion of adding more CUREs to the curriculum.
  4. The CURE's success prompted instructors to create a subsequent semester-long (follow-up) CURE.

How was administer buy-in achieved? Because the CURE is integrated into an existing course, a robust level of administrator buy-in is not usually required. We have anecdotal evidence that, for some instructors, PARE is appealing because they can "sneak" it into their curriculum in a way that is below the radar and/or non-threatening to non-supportive colleagues or administration.

Sustaining Change

What were the critical elements that made the CURE initiative sustainable? Sustainability was first and foremost on my mind when I created the program because I had heard from instructors involved in some other CUREs that they were disappointed when they could no longer run it when the funding ran out. I wanted to create something small and low cost with the hope that instructors would be able to implement it easily (low barrier). The hope was that after an initial implementation, they would have the personal confidence and perhaps administrative buy-in to enable them to extend the experience in subsequent years. This indeed did happen with a subset of instructors. We also started creating "extension modules" to appeal to those instructors who were interested in extending the research but did not feel they had the bandwidth to develop the extension research on their own.

We are currently investigating what the critical components are that make this CURE sustainable. We have not changed the nature of the core program since its inception, but we have added more modular opportunities that are now drawing interest on their own. Our evidence, to date, indicates that sustainability has to do with three factors: 1) it is short duration and easily compatible with existing course structure 2) its relatively low cost 3) and it is of broad interest to the students.

Were there any tipping points that facilitated the shift toward sustainability? There was never a "shift" as described in answer to the above. Because the program is very small in nature, it hasn't, thus far, required a major mindset shift of implementing instructors.

How has faculty buy-in been sustained? The fact that we continue to engage external researchers and create new modules likely serves to keep the interest of participating faculty. Many faculty also indicate that they appreciate the ability to take ownership of how the program evolves in their own classroom (due to its flexibility). Finally, we also try to create a very collaborative community among the participating instructors by providing agency to make suggestions for change, get involved in making the program better, etc.

Other than these items, we do not do anything specifically to address sustainability. We are generally approached only by instructors who have been seeking knowledge about implementing CUREs. In a few cases, these instructors are feeling pressure from their departments, but in most cases the drive is personal.

Who is teaching the CURE and how has that been sustained over time? The CURE has been implemented at about 125 undergraduate institutions, so instructors at each of these institutions have implemented. These instructors teach in a range of courses, often majors biology, majors microbiology or microbiology for allied health. Again, the CURE is designed to be inserted into an existing course, so the sustainability question is approached a bit differently than for a semester-long CURE.

We have done some tracking of faculty retention. The program is currently in its 6th year. In the third year, we tracked instructor retention and found it was at about 75%. Since then, we have not formally tracked retention, but we know that some instructors who left as of year 3 are now back teaching the CURE again.

Instructors who have left the CURE did so for two reasons. The first occurs when the instructor is no longer scheduled to teach the course in which the CURE was implemented. However, in these cases, the new instructor often continued using the CURE. The second occurs when the instructor left the CURE because they moved to a different institution. In at least two cases, those instructors found a way to implement the CURE in their new course at the new institution.

Why have you, as leader of the CURE initiative, stayed involved over time? I understand and have seen the empowerment that a research experience can provide to students, yet I am also moved by the number of undergraduates in the U.S. who may not have the opportunity to do research because their institutions do not have the infrastructure to support research. When I started, I had two personal goals, which remain my drivers. First, I wanted to create a low-barrier CURE that would be more accessible to community college instructors and those at very large institutions. Second, I wanted students to generate data with a particular goal in mind (i.e., identification of environmental sites that are "hotspots" for antimicrobial resistance and to be able to analyze that data to identify locations that might benefit from antimicrobial stewardship activities to prevent an outbreak of antibiotic resistant infections).

Advice for Implementation

What do you wish you had known when you started? I had been involved in the development of two CUREs prior, one of which was nationally disseminated. Based on this prior experience, I feel that I was prepared and I have not encountered any particular challenges in terms of dissemination. I have learned an enormous amount about how resources and administrative structure differ among institution types and how career goals and expected skills differ among student populations. These things would have been helpful to understand earlier on.

What advice would you give others who are just getting started with their CUREs? I learned from previous CURE development that expensive CUREs are difficult to sustain and disseminate and that semester-long CUREs, while terrific for the students, do require challenges that a modular CURE does not (e.g. new course approval, instructor "bandwidth"). I have also heard from countless instructors that the choice of research question should be relatable to the students. Our students repeatedly report that they enjoy knowing that they are working on a national research project because their work contributes to a larger effort. I feel that all of these factors should be considered when developing a new CURE program.

I would suggest if someone wants to develop a new CURE and have it be sustainable across many different institutions, they should consider overall costs, equipment needs, and try to make it compatible with existing course structure. I have learned a tremendous amount about the differences across institution types. For example, some faculty implement a few sections of a multi-section lab and their curriculum cannot deviate too much from the other sections. As another example, some community colleges are satellite campuses and need to keep their curriculum consistent across campuses. For semester-long CUREs, it is nearly essential that the CURE course provide credit toward graduation requirements. Finally, our instructors and students very commonly cite the broad relevance of our project as a motivator. The students love that they are contributing to a larger research project.