Antimicrobials are life-saving medications, and the use of these agents helps both treat and prevent infections. However, antimicrobial use is often unnecessary or suboptimal. Reference Magill, O’Leary and Ray1,Reference Fleming-Dutra, Hersh and Shapiro2 Unnecessary antimicrobial use provides no benefit to the patient but exposes the patient to potential antimicrobial-related harms. Suboptimal antimicrobial use may also contribute to patient harm, particularly if antimicrobials are underdosed, if less effective agents are prescribed, or if overly broad-spectrum agents are used when more narrow-spectrum agents would suffice.
A major consequence of unnecessary and suboptimal antimicrobial use is antimicrobial resistance, which is an urgent public health threat. To address this problem, the need to improve antimicrobial prescribing is widely recognized. The Centers for Disease Control and Prevention (CDC), the World Health Organization (WHO), and multiple other organizations have prioritized the need to improve antimicrobial use. 3,4 Since 2017, the Joint Commission has required that all accredited hospitals and nursing facilities have an antimicrobial stewardship program. In 2020, this requirement was also applied to all ambulatory healthcare organizations. In addition, the Centers for Medicaid and Medicare Services (CMS) has made the presence of an antimicrobial stewardship program a requirement for all participating hospitals and nursing facilities. Antimicrobial stewardship has 3 main goals: (1) optimizing clinical outcomes related to antimicrobial use, (2) minimizing toxicity and other adverse events related to antimicrobial use, and (3) limiting the emergence and spread of antimicrobial-resistant bacterial strains. 5
Efforts to improve antimicrobial prescribing are occurring within a changing healthcare landscape, which includes the rapid expansion of telehealth services. Since it was first introduced in the 1990s, telehealth has been seen as a tool for increasing access and improving the quality of care for people living in resource-limited areas. Reference Bashshur6 However, the uptake of telehealth has been slow, partly due to inadequate reimbursements for telehealth visits. Reference Mehrotra, Jena, Busch, Souza, Uscher-Pines and Landon7 Telehealth use has dramatically increased during the coronavirus disease 2019 (COVID-19) pandemic in many outpatient settings because minimizing in-person care is a way to reduce viral transmission. Before the COVID-19 pandemic, telehealth visits accounted for ˜1% of all primary care physician (PCP) visits. In the second quarter of 2020 when the COVID-19 pandemic hit the United States, telehealth visits increased to 35% of all primary care visits and the total number of primary care visits decreased significantly. Reference Alexander, Tajanlangit, Heyward, Mansour, Qato and Stafford8
In this review, we discuss how telehealth intersects with both inpatient and outpatient antimicrobial prescribing. By sharing infectious disease (ID) expertise and supporting antimicrobial stewardship processes, telehealth can help to improve inpatient antimicrobial use. We review the evidence supporting the use of telehealth for this purpose, including identified barriers. We also discuss the benefits of outpatient tele-ID consultations and the challenges to improving outpatient antimicrobial use within telehealth-delivered ambulatory care, such as primary and urgent care.
Definition of telehealth and telemedicine
The Healthcare and Public Health Sector Coordinating Council (HPH SCC) defines telehealth as “the use of telecommunications and information technology to provide access to health assessment, diagnosis, intervention, consultation, supervision, and information across distance.” Telemedicine is sometimes considered a subcategory of telehealth that refers to “the use of remote clinical services, encompassing diagnosis, treatment, and monitoring [of a patient].” 9 However, some authors and organizations, such as the American Telemedicine Association (ATA), use telehealth and telemedicine as interchangeable terms. Reference Hoffman10,Reference Tuckson, Edmunds and Telehealth11 In this review, we use the term “telehealth” to describe the use of telecommunications and information technology to deliver care to a patient or to provide advice to a provider across a geographic distance. To minimize confusion, we do not distinguish between telemedicine and telehealth.
Synchronous telehealth refers to telehealth provided via a real-time encounter using encrypted audiovisual communication; it allows for a patient–physician interaction similar to that of face-to-face visits. Asynchronous telehealth, also called “store and forward” telehealth, refers to a mode of telehealth that lacks live video or audio interaction. Relevant clinical information such as chief complaints, pertinent patient history, laboratory results, and images are sent to a remote specialist for review. Using the collected information, the specialist formulates a recommendation and communicates with the patient and/or the physician. Both synchronous and asynchronous telehealth can be used for ID consultations and antimicrobial stewardship.
Although some studies define electronic consultation (e-consultation) as consultations using both synchronous and asynchronous telehealth, we define e-consultations as consultations using asynchronous telehealth similar to a recent systematic review. Reference Vimalananda, Orlander and Afable12 We use the term “tele-ID consultation” to capture ID consultation using synchronous telehealth, asynchronous telehealth, or both.
Telehealth as a tool to improve inpatient antimicrobial prescribing
Telehealth can help share the expertise of ID specialists, including ID physicians, with resource-limited healthcare settings. Based on prior surveys, 41%–50% of US community hospitals lack an ID physician and 93% lack an ID-trained pharmacist. Reference Septimus and Owens13,Reference Reese, Gilmartin, Rich and Price14 Many facilities, especially hospitals that are too small or too remote to justify having an on-site ID specialist, would benefit from using telehealth. The Center for Disease Control and Prevention (CDC) guidelines on the implementation of antimicrobial stewardship in small and critical-access hospitals state that the use of telehealth should be considered. 15 The Infectious Diseases Society of America (IDSA) also supports appropriate and evidence-based use of telehealth to provide various kinds of ID services, including support for antimicrobial stewardship programs. Reference Siddiqui, Herchline and Kahlon16
Telehealth provides 2 avenues through which remote ID specialists can influence antimicrobial prescribing. First, remote ID specialists can support antimicrobial stewardship activities (ie, infectious diseases telehealth-supported antimicrobial stewardship, IDt ASP). Second, ID physicians can improve antimicrobial prescribing and associated clinical outcomes through direct tele-ID consultations. These 2 activities, which can be synergistic, work in different ways. Tele-ID consultation is initiated by a frontline physician’s consultation request. In contrast, IDt ASP can be a more proactive intervention because any patient on specific antimicrobials or with specific infectious diagnoses can be targeted without a frontline physician’s consultation request.
Telehealth-supported antimicrobial stewardship
Table 1 shows a summary of studies on the implementation of IDt ASPs. IDt ASPs provide evidence-based antimicrobial stewardship expertise without an on-site ID specialist. The approach of IDt ASPs can be modified depending on available platforms and resources. Most IDt ASPs implement the strategy of prospective audit and feedback (PAF) to optimize antimicrobial therapy, which is endorsed as a cornerstone antimicrobial stewardship activity by the CDC and the Joint Commission. 17,18 Prospective audit by ID telehealth (IDt) specialists can be achieved through remote or collaborative review with local caregivers and has been conducted at various frequencies (daily to biweekly). The IDt specialist must have EMR access for remote review, but if EMR access is lacking, the IDt specialist can collaboratively review the EMR with frontline caregivers. Communication of feedback and recommendations to frontline caregivers may be asynchronous (ie, EMR notes or e-mails) Reference Howell, Jacob and Mok19–Reference dos Santos, Deutschendorf, Carvalho, Timm and Sparenberg25 or synchronous (phone calls or teleconferences) with direct communication to local caregivers. Reference Knight, Michal, Milliken and Swindler26–Reference Vento, Veillette and Gelman30 All but 1 study involved a remote ID physician as a member of the IDt ASP. Reference Howell, Jacob and Mok19 The level of engagement of local caregivers in the IDt ASP can also vary; some programs identifying local ASP champions such as pharmacists, Reference Howell, Jacob and Mok19,Reference Stevenson, Banks and Stryczek21,Reference Yam, Fales, Jemison, Gillum and Bernstein22,Reference Laible, Grosdidier and Nazir27–Reference Ceradini, Tozzi and D’Argenio32 physicians, Reference Vento, Veillette and Gelman30 or infection preventionists, Reference Stevenson, Banks and Stryczek21,Reference Wilson, Banks and Crnich31 and others operate remotely and independently. In addition to PAF, some IDt ASPs provide didactic and case-based sessions led by IDt specialists during synchronous teleconferences. Reference Stevenson, Banks and Stryczek21,Reference Wilson, Banks and Crnich31 Participants in the teleconferences reported a positive experience, including a better understanding of the rationale for recommendations provided in real-time communications. Participants also felt that teleconferences enabled discussions between frontline clinicians and the stewardship team, which was preferable to asynchronous forms of communication. Reference Stevenson, Banks and Stryczek21
Table 1. Summary of Studies for Telehealth-Supported Antimicrobial Stewardship Program
Note. PAF, prospective audit and feedback; ID, infectious diseases; EMR, electronic medical record; ASP, antimicrobial stewardship program; VA: Veterans’ Affairs; CDI,Clostridioides difficile infection; DOT, days of therapy; AS, antimicrobial stewardship; IDt, infectious diseases telehealth; DDD, defined daily doses.
Studies on IDt ASPs have reported improved outcomes such as decreased inpatient antimicrobial use, Reference Wood, Nicolsen, Allen and Cook20,Reference Beaulac, Corcione, Epstein, Davidson and Doron23–Reference Knight, Michal, Milliken and Swindler26,Reference Shively, Moffa and Paul28–Reference Wilson, Banks and Crnich31 decreased cost related to inpatient antimicrobials, Reference Howell, Jacob and Mok19,Reference Yam, Fales, Jemison, Gillum and Bernstein22,Reference Ceradini, Tozzi and D’Argenio32 decreased Clostridioides difficile infections, Reference Yam, Fales, Jemison, Gillum and Bernstein22,Reference Beaulac, Corcione, Epstein, Davidson and Doron23 and improved antimicrobial susceptibility patterns of common organisms. Reference Wood, Nicolsen, Allen and Cook20,Reference Dos Santos, Dalmora and Lukasewicz24,Reference dos Santos, Deutschendorf, Carvalho, Timm and Sparenberg25,Reference Ceradini, Tozzi and D’Argenio32 One study also reported a 40% increase in ID consultations after the implementation of IDt ASP. Reference Shively, Moffa and Paul28
Several unique challenges have been identified in previous studies. First, the timeliness of remote ID specialists reviewing patients on active antimicrobials may be a barrier. Opportunities for improving antimicrobial prescribing can be missed if PAF is not performed frequently, especially when patient turnover is rapid. In one study, only 17% of recommendations were accepted, and 48% of stewardship recommendations were for patients who had already been discharged. Reference Howell, Jacob and Mok19 In this study, communication was delayed because a remote stewardship pharmacist reviewed cases at the end of each weekday and passed on recommendations to a local pharmacist, who might not have acted on the feedback until the following workday. Another barrier to IDt ASP could be technical difficulties, such as audio interference, especially at the beginning of implementation. Reference Stevenson, Banks and Stryczek21 Other barriers, not limited to telehealth, were limitations in resources and interference with other clinical duties. Reference Laible, Grosdidier and Nazir27
Overall, IDt ASPs appear to achieve outcomes similar to those of traditional antimicrobial stewardship programs. Further studies are needed to characterize the optimal model for IDt ASP activities and communications.
Telehealth for remote inpatient ID consultation
A summary of studies on tele-ID consultation is provided in Table 2. Telehealth has been used as an alternative way to consult with ID physicians for both hospitalized patients and patients in ambulatory care. For inpatient settings, tele-ID consultation has been used as a way to provide ID expertise for hospitals without an on-site ID physician. Reference Vento, Veillette and Gelman30,Reference Monkowski, Rhodes and Templer33–Reference Tande, Berbari and Ramar35 IDt specialists can provide advice on the initiation of empiric antibiotics, therapy modifications based on culture results and patients’ clinical response, or transfer to higher-level care when needed. Additionally, tele-ID inpatient consultations provide an opportunity for an ID physician to establish a therapeutic relationship with a patient, to arrange in-person or direct-to-consumer video follow-up visits and/or to arrange outpatient parenteral antimicrobial therapy.
Table 2. Summary of Studies for Tele-ID Consultation
Note. ID, infectious diseases; CI, confidence interval; ICU, intensive care unit; VA, Veterans’ Affairs; PCP, primary care physician; PCR, polymerase chain reaction; RVU: relative value unit.
Inpatient tele-ID consultation has been associated with fewer hospital transfers, Reference Monkowski, Rhodes and Templer33 shorter hospital length of stay Reference Monkowski, Rhodes and Templer33,Reference Assimacopoulos, Alam and Arbo34 and decreased 30-day mortality. Reference Tande, Berbari and Ramar35 Generally, physicians have been very satisfied with inpatient tele-ID consultation. Reference Vento, Veillette and Gelman30,Reference Tande, Berbari and Ramar35,Reference Canterino, Wang and Golden36 However, in one study, in which inpatient tele-ID consultation was used as an alternative to in-person ID consultation during the COVID-19 pandemic, ID consultants felt that the overall quality of tele-ID consultation was worse than traditional in-person ID consultation and that there are specific situations in which in-person consultation is necessary. Reference Canterino, Wang and Golden36
Access to patient EMRs, laboratory results, and imaging studies is necessary for both synchronous and asynchronous tele-ID consultation. In fact, all of the studies cited here were conducted in the same healthcare system in which remote ID specialists had full access to the EMR of the local hospitals. Reference Vento, Veillette and Gelman30,Reference Monkowski, Rhodes and Templer33–Reference Canterino, Wang and Golden36 For inpatient synchronous direct-to-consumer tele-ID consultation, a nurse or a local provider is often in the patient’s room, and additional equipment may be needed, such as in-room examination cameras or electronic stethoscopes. Reference Vento, Veillette and Gelman30,Reference Assimacopoulos, Alam and Arbo34 Some potential hurdles for implementing tele-ID consultation include medical licensure, medical liability insurance, and reimbursement across state lines. Reference Abdel-Massih and Mellors37 Because tele-ID consultations are often combined with IDt ASP, offering an annual subscription to both telehealth service may be a good model. Reference Vento, Veillette and Gelman30
Integration of tele-ID consultation and telehealth-supported antimicrobial stewardship
Hospitals can simultaneously implement tele-ID consultation and IDt ASP. In fact, combined IDt ASP and e-consultation, called a videoconference antimicrobial stewardship team (VAST), was successfully implemented at 2 medical centers in the Veterans’ Affairs health system. Reference Stevenson, Banks and Stryczek21,Reference Wilson, Banks and Crnich31 In the VAST program, a remote ID physician provided input on selected ID cases during weekly video conferences with local hospital staff members. Reference Wilson, Banks and Crnich31 Similarly, Vento et al Reference Vento, Veillette and Gelman30 described integrated ID telehealth services, which included tele-ID consultation and IDt ASP.
Previous studies have suggested that antimicrobial stewardship activities stimulate formal ID consultation rather than replace it. Reference Suzuki, Perencevich and Goto38,Reference Morrill, Gaitanis and LaPlante39 Likewise, both telehealth-supported antimicrobial stewardship and e-consultation have increased the number of total ID consultations without decreasing the number of in-person ID consultations. Reference Shively, Moffa and Paul28,Reference Stenehjem, Hersh and Buckel29,Reference Strymish, Gupte and Afable40
Notably, for complicated cases, in-person ID consultation has distinct advantages to remote, telehealth reviews. However, a recent retrospective study reported that tele-ID consultation was as effective as in-person ID consultation for patients with Staphylococcus aureus bacteremia when a care bundle for S. aureus bacteremia had already been implemented by the local antimicrobial stewardship team. Reference Meredith, Onsrud and Davidson41 This study highlights the importance of collaboration between tele-ID consultation and telehealth-supported antimicrobial stewardship activities.
Telehealth and outpatient antimicrobial use
Telehealth to access ID expertise for outpatients
In outpatient settings, e-consultations can be used to more rapidly access ID expertise (Table 2). Reference Vento, Veillette and Gelman30,Reference Strymish, Gupte and Afable40,Reference Gonzalez, Sabella and Esper42–Reference Murthy, Rose, Liddy, Afkham and Keely44 Similar to inpatient tele-ID consultation, referring physicians expressed satisfaction with e-consultations either by learning additional information that affected patient care or by receiving validation of their management decisions. Reference Murthy, Rose, Liddy, Afkham and Keely44 Interestingly, a large number of outpatient e-consultations were related to questions that had previously been posed to ID consultants via curbside consultations; these informal discussions did not involve the consultant seeing the patient or reviewing the EMR. Questions centered around the interpretation of laboratory results, antimicrobial recommendation for positive microbiology results, vaccinations, or particular exposures. In fact, one study reported a decreased number of curbside ID consultations after implementation of outpatient e-consultations. Reference Wood, Bender and Jackson43 Therefore, outpatient e-consultation can be regarded as a preferable alternative to telephone calls, which can increase access to ID expertise rather than replace in-person ID consultation.
One study implemented direct-to-consumer synchronous telehealth as a way to expand ID expertise to outpatients in a remote region where most of the population was part of First Nations communities. Reference Mashru, Kirlew, Saginur and Schreiber45 Over the course of 1 year, this project provided both direct patient care and held case conferences with providers. Patient satisfaction was high.
Antimicrobial stewardship opportunities for telehealth-delivered primary, urgent, and emergency department care
Telehealth is increasingly used as a tool for providing care in outpatient settings, including primary care, urgent care, and emergency departments. Telehealth visits in ambulatory care offer opportunities for antimicrobial stewardship. Some challenges to improving antimicrobial use in these telehealth visits are new, and other challenges are similar to those encountered in more traditional outpatient settings.
Factors affecting antimicrobial prescribing in outpatient telehealth visits
The decision to prescribe antimicrobials in an outpatient setting is a complex issue influenced by many external and internal factors. Based on prior studies of face-to-face encounters in ambulatory care, physician factors that contribute to antimicrobial overuse include knowledge deficits or lack of familiarity with treatment guidelines, diagnostic uncertainty, and a desire to ensure patient satisfaction. Reference Rose, Crosbie and Stewart46 In addition to physician factors, antimicrobial prescribing can be affected by patient factors. For example, patient pressure or expectation to receive antimicrobials can lead to antimicrobial overprescription. Other patient factors include patient comorbidities (immunosuppression, etc), socioeconomic status, and communication barriers. External factors, such as organizational pressure for financial incentives, further complicate the decision making for antimicrobial prescribing. Physicians may elect to prescribe antimicrobials to see more patients rather than taking more time to explain why antimicrobials are not indicated.
Most of the aforementioned factors, which were identified from research on face-to-face encounters, may hold true in the setting of telehealth, but some factors may be stronger and others may be weaker. Gomez et al Reference Gomez, Anaya, Shih and Tarn47 conducted a qualitative study to assess physician perspectives on telehealth. Primary care physicians uniformly stated that their inability to perform a physical examination is a major disadvantage to telehealth, and some also thought that this could lead to antimicrobial overprescribing. In the same study, several physicians stated that they felt more comfortable refusing patient requests for unnecessary antimicrobials during telehealth visits compared to face-to-face visits.
Previous studies about frontline providers’ antimicrobial prescribing via telehealth
Several studies have compared frontline providers’ antimicrobial prescribing via telehealth and face-to-face visits with mixed results. These studies varied in the type of telehealth, type of face-to-face visits, and infectious diagnoses for which antimicrobials were prescribed; settings included primary care, urgent care, emergency care, and retail clinics. A systematic review and meta-analysis of studies that compared antimicrobial prescribing via telehealth and face-to-face encounters for common outpatient infections found that antimicrobials were more frequently prescribed via telehealth compared to face-to-face visits for patients with otitis media (pooled odds ratio [OR], 1.26; 95% confidence interval [CI], 1.04–1.52) and pharyngitis (pooled OR, 1.16; 95% CI, 1.01–1.33). Reference Suzuki, Marra and Hasegawa48 No significant differences were observed between the 2 modes of delivery for sinusitis and upper respiratory infection (URI). Across both modes of care delivery, antimicrobials were prescribed for 30%–40% of patients with URI, an infection in which antimicrobials are almost never indicated, and antimicrobials were prescribed for 60%–70% of patients with sinusitis, otitis media, and pharyngitis—3 infections that are frequently viral. Due to significant heterogeneity across the included studies, these results need further validation. Nevertheless, these findings suggest that antimicrobials are commonly overprescribed in outpatient settings and might be further overprescribed via telehealth for diagnoses in which physical examination is a necessary part of evaluation, such as otitis media and pharyngitis. It is possible that increased diagnostic uncertainty due to the lack of physical examination resulted in more antimicrobial use, but there is a need for more research to understand how antimicrobial decision making in telehealth differs from decision making in face-to-face encounters.
Strategies to improve outpatient providers’ antimicrobial prescribing for telehealth encounters
Conventional outpatient antimicrobial stewardship strategies might also be effective in telehealth settings that replace traditional primary, urgent care, or emergency room care. All of the CDC core elements for outpatient antibiotic stewardship are applicable to the telehealth setting. 49 In addition, many policies or practices, such as delayed prescribing or requiring written justification, can be applied in the EMR and will work for both telehealth and face-to-face visit settings.
However, research on implementing stewardship strategies within the context of telehealth encounters is limited. In a study across a primary care network in western Michigan, a computerized decision support system (CDSS) was leveraged as a stewardship strategy. This CDSS guided physicians to the correct diagnosis and treatment using drop-down menus of guideline-based treatment options. The authors observed significantly more guideline-concordant diagnoses (69.1% vs 45.7%) and less antimicrobial prescribing (68.6% vs 94.3%) for patients with sinusitis in telehealth compared to face-to-face visits. Reference Johnson, Dumkow, Burns, Yee and Egwuatu50 Similarly, patients with urinary tract infection seen via telehealth were more likely to receive firstline antibiotic agents (74.9% vs 59.4%) and a guideline-concordant duration of therapy (100% vs 53.1%) compared to those seen via face-to-face visits. Reference Johnson, Dumkow, Salvati, Johnson, Yee and Egwuatu51
Pedrotti et al Reference Pedrotti, Accorsi and De Amicis Lima52 described antibiotic-prescribing practices during synchronous direct-to-consumer telehealth for outpatient visits in Brazil. All telehealth doctors were general practitioners; they were trained on antibiotic stewardship protocols, monitored by senior supervisors, and provided bimonthly feedback on their protocol adherence. Within this framework, rates of antimicrobial prescribing were low for conditions that never or frequently do not require antibiotics, such as URIs (2.5% received antimicrobials), pharyngo-tonsillitis (35% received antimicrobials), acute sinusitis (51.8% received antimicrobials), and acute diarrhea (1.6% received antimicrobials).
Although most outpatient antimicrobial stewardship interventions may work for antimicrobial prescribing via telehealth, the adoption of antimicrobial stewardship in outpatient settings, in general, continues to lag. 53 Continued efforts to expand the reach of outpatient antimicrobial stewardship activities will likely lead to improved antimicrobial prescribing via telehealth. In addition, it is important to acknowledge that patients with some diagnoses that require physical examination may be at risk for antimicrobial overprescribing when seen via telehealth. Additional measures should be undertaken to avoid this risk. One possible solution is to deploy tools that enable remote physical examination, such as a remote stethoscopes or remote otoscopes. Another solution would be to develop guidelines for schedulers and triage officers to guide decisions about types of visits that are appropriate for telehealth versus face-to-face visits. Reference Gomez, Anaya, Shih and Tarn47
In this narrative review, we have discussed how telehealth can provide access to remote ID specialists and, in turn, can be an effective tool for improving both antimicrobial use and clinical outcomes in patients treated with antimicrobials. There is tremendous potential to expand the reach of ID specialist and antimicrobial stewardship expertise through telehealth, but additional research is needed to define optimal strategies for implementing this technology and to adapt it to different local settings.
Routine medical care delivered via telehealth also presents new challenges and opportunities for efforts to promote antimicrobial stewardship. It is unclear whether existing stewardship strategies may transfer easily from the face-to-face to the telehealth setting. The increased adoption of telehealth during the COVID-19 pandemic will probably encourage high levels of telehealth use even after the pandemic has ended. Reference Weiner, Bandeian, Hatef, Lans, Liu and Lemke54 Given the continued use of telehealth services and the urgent public health threat of antimicrobial resistance, further work is needed to evaluate the effectiveness and optimal implementation of stewardship strategies within these types of encounters.
Acknowledgments
We thank Dr Todd Vento for his thoughtful input about telehealth. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the Department of Veterans’ Affairs or the US government.
Financial support
No financial support was provided relevant to this article.
Conflicts of interest
All authors report no conflicts of interest relevant to this article.
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