Highlights
- •Studies suggest that telemedicine (TM) increases antibiotic prescription rate.
- •We analyzed 6050 TM visits performed under rigorous antibiotic stewardship.
- •Most acute low-risk infectious conditions were adequately managed by TM.
- •TM under stewardship was associated with low and adequate antibiotic prescription.
Abstract
Objective
To analyze the antibiotic prescription rate in low-risk patients evaluated at a telemedicine program that adopts antibiotic stewardship protocols.
Methods
Adult patients who accessed a single direct-to-consumer telemedicine center (Jan/2019–Feb/2020) were retrospectively enrolled. Diseases amenable to antimicrobial treatment were classified under five diagnostic groups: upper respiratory tract infection (URI), acute pharyngotonsillitis (PT), acute sinusitis (AS), urinary tract infection (UTI), and acute diarrhea (AD). Physicians were trained on and advised to strictly follow the current guideline recommendations supported by institutional antibiotic stewardship protocols, readily available online during consultations. We analyzed the antibiotic prescription rate among patients, referral rate, and antibiotic class through descriptive statistics.
Results
A total of 2328 patients were included in the study. A total of 2085 (89·6%) patients were discharged with usual recommendations, medication (if needed), and instructions about red flags, while 243 (10·4%) were referred to a face-to-face consultation. Among the discharged patients, the antibiotic prescription rates by the diagnostic group were URI — 2·5%, PT — 35·0%, AS — 51·8%, UTI — 91.6%, and AD — 1·6%. In most cases, prescribed antibiotics were in line with institutional stewardship protocols.
Conclusions
Low prescription rate of antibiotics can be achieved using antibiotic stewardship protocols at direct-to-consumer telemedicine consultations, showing high adherence to international guidelines. These results reinforce telemedicine as a cost-effective and safe strategy for the initial assessment of acute non-urgent symptoms.
Keywords
Introduction
Annual emergency department (ED) visits increase each year, and according to the National Hospital Ambulatory Medical Care Survey, in 2017, total ED visits reached almost 140 million only in the US (
Pulia et al., 2018
). Furthermore, a recent US healthcare system analysis concluded that about half of all medical care occurs at ED, and infection is one of the most common final diagnoses (Marcozzi et al., 2018
). During infection-related ED visits, antimicrobial agents are one of the most prescribed drugs. The US Centers for Disease Control and Prevention estimates that EDs generated more than 28 million antibiotic prescriptions in 2015 (Rui and Kang, 2017
).When indicated by current guidelines, antibiotic prescription is associated with lower morbidity in many low-risk conditions, and timely prescription can be lifesaving in high-risk patients (
Sherwin et al., 2017
). However, unnecessary or inappropriate prescriptions are common, particularly in low-risk situations, and can lead to community and patient hazards, including antimicrobial resistance, treatment failure, and adverse events (Denny et al., 2016
). At least 20% of patients present antibiotic-associated adverse drug events (Tamma et al., 2017
). Unfortunately, there are few published studies on the appropriateness of prescribing antibiotics. A recent survey at a US Veterans Affairs ED found that 39% of antimicrobial use was potentially inappropriate (Timbrook et al., 2017
).The increasing healthcare cost of unnecessary ED visits promotes the development of more accessible and more cost-effective alternative acute care venues such as retail clinics, urgent care centers, and, more recently, telemedicine (
Poon et al., 2018
). However, one of the main concerns is that the broader availability of these alternatives, particularly telemedicine, could cause an increase inappropriate antibiotic prescription rates (Uscher-Pines et al., 2015
).Nevertheless, the adoption of telemedicine, in general, is growing and provides obvious benefits for patients, including convenience and lower costs (
Ray et al., 2019a
). As expected, telemedicine visits in which the main symptoms may lead to antibiotic prescriptions are standard. A study showed that 55% of the visits resulted in antibiotics being prescribed, which is consistent with other recent studies (Timbrook et al., 2017
). Broad-spectrum antibiotics (such as amoxicillin–clavulanate, cefdinir, and azithromycin) made up more than one-third of the antibiotics prescribed (Agiro et al., 2018
). Furthermore, the higher rate of antibiotics prescription can be ascribed to higher immediate satisfaction rates, which may create higher psychological pressure on physicians to prescribe more antimicrobial drugs (Baummer-Carr and Nicolau, 2017
). Conflicting evidence shows that antibiotic-prescribing rates for acute respiratory infections are similar or higher for patients who consulted telemedicine services than those who had face-to-face visits (Yao et al., 2020
). There are still worries that telemedicine, due to its wider availability and affordability, could lead to a more liberal antibiotic prescription (Ray et al., 2019b
).To date, most papers that addressed antibiotic prescription through telemedicine did not specify the protocols and guidelines that are accessible to doctors or how the doctors should be trained and monitored for antibiotic stewardship (
Zetts et al., 2018
). The adherence to practice guidelines (for choosing the proper antibiotic class and indication) for multiple infectious diseases diagnosed by emergency telemedicine assessment is not well studied. This study aims to quantify and characterize the antibiotic prescription rates according to institutional stewardship protocols at a high-volume single telemedicine center for five diagnostic groups in which an antimicrobial agent may be considered—namely, upper respiratory tract infection (URI), acute pharyngotonsillitis (PT), acute sinusitis (AS), urinary tract infection (UTI), and acute diarrhea (AD).Material and methodologies
Study design and participants
The local institutional review board approved this study. All patients had access to telemedicine services provided by Hospital Israelita Albert Einstein (Sao Paulo, Brazil) through a web-based mobile application and made spontaneous medical evaluation requests. All consultations were video-based, with a board-certified general practitioner. Antibiotic stewardship protocols were based on the best current evidence, and local guidelines were adapted to video-based consultations and were developed and made readily and universally available in electronic format to be used whenever needed (Table 1). All telemedicine doctors were required to be trained on those protocols, and senior supervisors monitored antibiotic prescription rates. All telemedicine physicians receive bi-monthly feedback regarding adherence to guidelines and reorientation if necessary.
Table 1Antibiotic prescription institutional stewardship guidelines.
| Group | Antibiotic prescription criteria | Referral criteria (red flags) | Recommended first option antibiotic | Ref. |
|---|---|---|---|---|
| AD | Travel diarrhea, severe symptoms | High-grade fever, blood or mucus in stool, severe abdominal pain, severe vomiting | Ciprofloxacin 500 mg bid for 3 days | Riddle et al., 2016 |
| AS | Symptoms not improving for 10+ days, severe symptoms for 3–4+ days, double-sickening pattern | High-grade persistent fever, respiratory distress, periorbital edema, proptosis, facial erythema, visual symptoms | Amoxicillin + clavulanate 875/125 mg bid for 7 days | Chow et al., 2012 |
| PT | FeverPAIN score ≥3 | Respiratory distress, signs of airway obstruction, signs of tonsillar abscess, stiff neck | Amoxicillin 875 mg bid for 10 days | Shulman et al., 2012 |
Windfuhr et al., 2016 | ||||
Oliver et al., 2018 | ||||
Fraser et al., 2020 | ||||
| URI | None | High-grade persistent fever, persistent cough, the sign of respiratory distress | None | Kenealy and Arroll, 2013 |
| UTI | Female, reproductive age, with no signs of systemic involvement | Male gender, fever, back pain, signs of systemic involvement, severe hematuria, vulvovaginal symptoms | Fosfomycin 3 g single dose | Colgan et al., 2011 |
Nicolle, 2014 | ||||
Takhar and Moran, 2014 | ||||
Rastogi et al., 2020 |
AD, acute diarrhea; AS, acute sinusitis; PT, acute pharyngotonsillitis; URI, acute upper respiratory infection; UTI, urinary tract infection.
a If referral criteria were present, the patient was referred to an urgent face-to-face visit. Age over 75, multiple comorbidities, and severe limitation of daily activities were also considered red flags for all diagnostic groups.
Between January 2019 and February 2020, all patients ≥18 years who sought consultations for acute, on-demand telemedicine assessment were retrospectively enrolled for this study. The inclusion criterion was the presence of any acute symptom. Asymptomatic patients who requested an evaluation for guidance, chronic drug prescriptions, or diagnostic tests were excluded. According to clinical judgment, all eligible patients received a diagnosis based on ICD-10 and had their destination defined as discharge or ED referral. For the aggregation of most prevalent infectious diseases with similar pathophysiologic characteristics, five diagnostic groups were defined based on ICD-10 codes: (1) URI—Acute Upper Respiratory Infection (J00, J04, J06, J39); (2) PT—Acute Pharyngotonsillitis (J02–J03.9); (3) AS—Acute Sinusitis (J01–J01.9); (4) UTI—Urinary Tract Infection (N30, N39.0); (5) AD—Acute diarrhea (A00–A09). ICD-10 codes that refer only to symptoms are not commonly used in this service. A presumptive diagnostic code was given if the patient had to be referred to an urgent face-to-face consultation by protocol or clinical judgment. The primary endpoint was the antibiotic prescription rate among patients not referred to in-person consultation in each diagnostic group. The characterization of the antibiotic class and ED referral rate were secondary endpoints in this analysis.
Statistical analysis
The present study was an observational, retrospective, cross-sectional analysis, and all statistics were only descriptive. Age was expressed as median value, and interquartile rates (IQR) and the categorical variables were presented as counts and percentages.
Results
Between January 2019 and February 2020, 6050 telemedicine visits were performed (14,2 visits/day). A total of 2348 (38.8%) visits were included in one of the five specified diagnostic groups. Twenty (0·9%) of these were excluded by technical problems. Two-hundred and forty-three (10·4%) patients were referred for a face-to-face consultation. Thus, for 2085 (89·6%) patients, teleconsultation alone was considered safe and enough for patient management by institutional protocols. The selected patients were distributed into five diagnostic groups: URI—788 (37·8%), AD—488 (23.4%), PT—386 (18·5%), AS—197 (9·4%), and UTI—226 (10·8%). Of these patients, antibiotics were prescribed to 22·6% (472) patients distributed across diagnostic groups: 1. URI—2·5% (n = 788), 2. PT—35·0% (n = 386), 3. AS—51·8% (n = 197), 4. UTI—91·6% (n = 226), and 5. AD—1·6% (n = 488). The study population’s median age was 34 years (IQR 28–40), and 39·2% were male. In the study population, diagnostic groups’ referral rates were URI—5·6%, PT—9.0%, AS—7·5%, UTI—23·1%, and AD—13·2% (details in Table 2).
Table 2Diagnostic groups distribution, gender, and ED referrals.
| Group | N | % | Male | % Male | ED Referral | % ED Referral |
|---|---|---|---|---|---|---|
| AD | 562 | 24·1% | 243 | 43·2% | 74 | 13·2% |
| AS | 213 | 9·1% | 84 | 39·4% | 16 | 7·5% |
| PT | 424 | 18·2% | 203 | 47·9% | 38 | 9·0% |
| URI | 835 | 35·9% | 363 | 43·5% | 47 | 5·6% |
| UTI | 294 | 12·6% | 19 | 6·5% | 68 | 23·1% |
| Total | 2328 | 100·0% | 912 | 39·2% | 243 | 10·4% |
AD, acute diarrhea; AS, acute sinusitis; PT, acute pharyngotonsillitis; URI, acute upper respiratory infection; UTI, urinary tract infection.
Beta-lactams were the most prescribed antibiotic class. They accounted for 45.6% of all antibiotic prescriptions and were prescribed mainly for PT. The second most prescribed antibiotic class was fosfomycin (29·7%), prescribed only for UTI. It was noted that there was an excellent adherence to guidelines recommendations, with a low antibiotic prescription rate for URI and AD. The predominant prescription for PT was beta-lactams, also preferred for AS, and a strong preference was seen for fosfomycin for UTI (details in Table 3). Only 38 (1.8%) patients received a quinolone prescription, representing 8.1% of all antibiotics prescribed.
Table 3Antibiotic prescription rate and antibiotic class.
| Group | Antibiotic | Beta-Lactam | Macrolide | Cephalosporin | Fosfomycin | Quinolone | Other |
|---|---|---|---|---|---|---|---|
| AD | 8 (1·6%) | 1 (12·5%) | 0 (0·0%) | 0 (0·0%) | 0 (0·0%) | 5 (62·5%) | 2 (25·0%) |
| AS | 102 (51·8%) | 91 (89·2%) | 3 (2·9%) | 5 (4·9%) | 0 (0·0%) | 3 (2·9%) | 0 (0·0%) |
| PT | 135 (35·0%) | 106 (78·5%) | 24 (17·8%) | 3 (2·2%) | 0 (0·0%) | 0 (0·0%) | 2 (1·5%) |
| URI | 20 (2·5%) | 12 (60·0%) | 7 (35·0%) | 1 (5·0%) | 0 (0·0%) | 0 (0·0%) | 0 (0·0%) |
| UTI | 207 (91·6%) | 5 (2·4%) | 2 (1·0%) | 13 (6·3%) | 140 (67·6%) | 30 (14·5%) | 19 (9·2%) |
| Total | 472 (22·6%) | 215 (45·6%) | 36 (7·6%) | 22 (4·7%) | 140 (29·7%) | 38 (8·1%) | 23 (8·1%) |
AD, acute diarrhea; AS, acute sinusitis; PT, acute pharyngotonsillitis; URI, acute upper respiratory infection; UTI, urinary tract infection.
Discussion
The evaluation of patients with acute, low acuity symptoms in emergency care units is surrounded by circumstances that can influence diagnostic accuracy (
Di Somma et al., 2015
). Imprecision of the patient’s personal history, crowded services, professional burnout, absence of necessary additional tests, and many interruptions during caregiving are some of the impediments commonly experienced in an ED. Despite the possibility of a complete physical evaluation adding to the diagnostic value, many symptoms are compatible with low-risk situations, and irrelevant routine examination is standard (Sahota and Lang, 2017
). The patient’s psychological profile and pressure for specific management are also factors associated with the treatment change (Lauria et al., 2016
). These multiple factors may imply low adherence to the plethora of current guidelines (Fernández Mondéjar, 2017
). Balancing patient demands during care with the full spectrum of severity and frequent interruptions creates time pressures that predispose humans to rapid thoughts or cognitive shortcuts, including cognitive biases, leading professionals to misdiagnoses (Kahneman, 2003
). Methods to monitor these errors at ED are fundamental to establishing the frequency of errors and serve as a basis for interventions that aim to minimize these errors (Medford-Davis et al., 2018
).Among the patient’s main reasons to visit an ED, acute infectious diseases are among the most frequent (
Marcozzi et al., 2018
). Due to the stress mentioned above and as an attempt to rapidly meet patients’ demands, antibiotic prescriptions are standard, often unnecessary, and possibly harmful (Denny et al., 2016
). To minimize these interventions, institutional support and appropriate antibiotic stewardship protocols can guide antimicrobial administration in the ED to avoid the prescription of antibiotics in conditions not indicated in the respiratory tract, such as URIs and other situations (Denny et al., 2016
).Like common-cold, URIs are among the most common acute illnesses leading to urgent consultations in developed countries and account for a substantial economic burden. Being mostly self-limited and caused by viruses, systematic reviews and meta-analyses have found no role for prescribing antibiotics for its treatment, and such prescription may significantly increase the adverse event rates and potential harm (
Kenealy and Arroll, 2013
). With only a 2.5% antibiotic prescription rate for URIs, this study shows that exceptionally close adherence to guidelines can be achieved in direct-to-consumer telemedicine with well-conducted stewardship.PT is another common reason for people to visit primary care centers and EDs. Surveys have found that up to 10% of the population may look for medical attention each year reporting a sore throat (
Windfuhr et al., 2016
). Although it is advised that clinical management may be guided by well-validated clinical criteria and antigen testing (now widely available in developed countries), antibiotics are still prescribed to most patients presenting an acute sore throat. Frequently caused by a virus (mainly rhinovirus), the distinction between the viral and bacterial PT can be clinically challenging (Oliver et al., 2018
). In Brazil, where the availability of antigen testing for Streptococcus is almost nil, most guidelines suggest using a validated clinical scoring system to guide antibiotic prescription. Easily applicable to telemedicine consultations, our clinical protocol includes the FeverPAIN score, suggesting immediate antimicrobial agent prescription only for a score of 3 or higher (Fraser et al., 2020
). Although many guidelines advise empiric antibiotics with a 4 and higher score, we adapted to a more sensitive approach due to the higher local incidence of rheumatic fever and antigen tests’ unavailability. A 35% antibiotic prescription rate for PT can then be considered low compared to other telemedicine programs.Acute sinusitis is an important and frequent low acuity diagnosis responsible for over 3 million outpatients visits annually only in the US. About 75% of patients will receive an antibiotic prescription, even though bacteria cause only about one-third of infections (
Fleming-Dutra et al., 2016
). Our protocol suggests avoiding an antibiotic for AS if symptoms are not severe or long-lasting, based on international guidelines (Chow et al., 2012
). The prescription rate was 51.8%, suggesting that there is still room for improvement, although the actual rate may be less because less severe symptoms could lead to a URI diagnosis (ICR code J00 or J06) instead of an ICD J01 code.UTI, mainly in young women, is also commonly found in the context of the emergency department, with more than 250,000 cases reported each year in the US (
Colgan et al., 2011
). Differentiating lower tract UTI and upper tract UTI is predominantly based on history and examination. The clinical diagnosis of cystitis is made with classic signs and symptoms (i.e., dysuria, urinary frequency, urgency, or suprapubic pain) (Takhar and Moran, 2014
). In most clinical scenarios, urinary testing may not be required if the patient meets the criteria for uncomplicated cystitis, and an empirical antibiotic prescription is usually recommended, with a preference for narrower spectrum antibiotic classes. In our telemedicine service, 23.1% were referred to an ED consultation, mostly due to red flags indicating a higher risk of acute pyelonephritis. For the remaining 76.9%, an antibiotic was prescribed in 91.6% of cases. As the clinical history is based on a simple physical examination, findings from such examination are the main elements used in telemedicine to raise a diagnostic hypothesis. Typical cystitis symptoms were associated with a high prescription of antibiotics and may have reduced the prescription of these drugs in asymptomatic bacteriuria. This condition generally does not need treatment, except in special conditions such as pregnancy and for patients undergoing urologic procedures (Nicolle, 2014
). Most patients diagnosed with a UTI were prescribed an appropriate antibiotic, most frequently fosfomycin (67.6%). Our first option is fosfomycin for the convenience of its administration being in a single dose, high TMP-SMX resistance in Brazil, and nitrofurantoin being available only in macro-crystal formulation makes it less tolerable and the dosing schedule unsuitable. We still had a quinolone prescription rate of 14.5% of the total UTI cases. This value is similar to that in another study in the literature that presented a 10% quinolone prescription rate. This article highlights that a small portion of physicians prescribed quinolones more than 30% of the time, suggesting that inappropriate prescribing is limited to a few outliers (Rastogi et al., 2020
). The last diagnostic group considered in this study consisted of AD patients. This accounts for over 179 million cases annually in the US and a frequent reason for ED and primary care visits. Although widely prescribed, antibiotics are reserved for only a small percentage of cases, mostly sporadic febrile dysentery with signs of systemic involvement and severe travelers’ diarrhea (Riddle et al., 2016
). In our cohort, only 1.6% of the discharged patients received an antibiotic prescription, mostly ciprofloxacin. This abnormally low rate may be explained by the fact that the patients eligible for antibiotics also presented red flags that caused them to be referred to an in-person consultation, which in our case was 13.2%. Nevertheless, for the remaining 86.8% of the patients, the low prescription rate was still remarkable.In general, the overall referral rate was low, and physicians mostly followed the designed protocols for antibiotic prescription and antibiotic class choice. Our institution has adopted objective protocols specifically designed for telemedicine, with easy access directly from the electronic health records interface, describing the red flags upon which the patient should be referred to the ED and suggesting when antibiotics should be prescribed. All medical records are reviewed monthly using natural language processing algorithms for protocol adherence, and potential management divergences are annotated and discussed in individual interviews with attending physicians. This study shows that using technology and proper antibiotic stewardship may mitigate the apprehension that video visits may lead to a high antibiotic prescription rate.
Conclusion
Among patients with acute, low acuity symptoms visiting direct-to-consumer telemedicine service for consultations, a low rate of an inappropriate antibiotic prescription can generally be achieved using antibiotic stewardship protocols and close adherence to the international guidelines. Telemedicine is to be reinforced as a cost-effective and safe strategy for the initial assessment of acute non-urgent symptoms.
Conflict of interests
The authors declare that they have no financial or personal interests that could have influenced the work.
Funding
None.
Ethical approval
This study was approved by the Hospital Israelita Albert Einstein review board (30594920.4.0000.0071).
Acknowledgments
The authors want to thank the Hospital Israelita Albert Einstein for the information technology support relating to the relevant services (telemedicine) provided.
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Article info
Publication history
Published online: February 09, 2021
Accepted:
February 5,
2021
Received in revised form:
February 3,
2021
Received:
December 4,
2020
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