








key: cord-330545-jrmott3i
authors: Abuzeineh, Mohammad; Muzaale, Abimereki D.; Crews, Deidra C.; Avery, Robin K.; Brotman, Daniel J.; Brennan, Daniel C.; Segev, Dorry L.; Al Ammary, Fawaz
title: Telemedicine in the Care of Kidney Transplant Recipients with COVID-19: Case Reports
date: 2020-07-16
journal: Transplant Proc
DOI: 10.1016/j.transproceed.2020.07.009
sha: 
doc_id: 330545
cord_uid: jrmott3i

Abstract Kidney transplant recipients who develop symptoms consistent with COVID-19 are bringing unique challenges to health care professionals. Telemedicine has surged dramatically since the pandemic in efforts to maintain patient care and reduce the risk of COVID-19 exposure to patients, healthcare workers, and the public. Herein we present reports of three kidney transplant recipients with COVID-19 that were managed using telemedicine via synchronous video visits integrated with an electronic medical records system, from home to inpatient settings. We demonstrate how telemedicine helped assess, diagnose, triage, and treat patients with COVID-19 while avoiding an emergency room or outpatient clinic visit. While there is limited information about the duration of viral shedding for immunosuppressed patients, our findings underscore the importance of using telemedicine in the follow-up care for kidney transplant recipients with COVID-19 who have recovered from symptoms but might have persistently positive NAT tests. Our experience emphasizes the opportunities of telemedicine in the management of kidney transplant recipients with COVID-19 and in the maintenance of uninterrupted follow-up care for such immunosuppressed patients with prolonged viral shedding. Telemedicine may help increase access to care for kidney transplant recipients during and beyond the pandemic as it offers a prompt, safe, and convenient platform in the delivery of care for these patients. Yet in order to advance the practice of telemedicine in the field of kidney transplantation, barriers to increasing the widespread implementation of telemedicine should be removed, and research studies to assess the effectiveness of telemedicine in the care kidney transplant recipients are needed.

that were managed using telemedicine via synchronous video visits integrated with an electronic medical records system, from home to inpatient settings. We demonstrate how telemedicine helped assess, diagnose, triage, and treat patients with COVID-19 while avoiding an emergency room or outpatient clinic visit. While there is limited information about the duration of viral shedding for immunosuppressed patients, our findings underscore the importance of using telemedicine in the follow-up care for kidney transplant recipients with COVID-19 who have recovered from symptoms but might have persistently positive NAT tests. Our experience emphasizes the opportunities of telemedicine in the management of kidney transplant recipients with COVID-19 and in the maintenance of uninterrupted follow-up care for such immunosuppressed patients with prolonged viral shedding.

Telemedicine may help increase access to care for kidney transplant recipients during and beyond the pandemic as it offers a prompt, safe, and convenient platform in the delivery of care for these patients.

Yet in order to advance the practice of telemedicine in the field of kidney transplantation, barriers to increasing the widespread implementation of telemedicine should be removed, and research studies to assess the effectiveness of telemedicine in the care kidney transplant recipients are needed.

• Telemedicine helped diagnose, triage, and manage transplant patients with COVID-19

• Practical workflow process for COVID-19 test and surveillance

• Telemedicine aid from home to inpatient settings, while avoiding ER or clinic visit

• Telemedicine provides prompt, safe, and convenient approach to COVID-19 patients Kidney transplant recipients who develop symptoms consistent with COVID-19 are bringing unique challenges to health care professionals. 1,2 While the potential for both community and nosocomial spread of COVID-19 when such patients seek care is a major concern, proper diagnosis and management of these patients must be accommodated. [3] [4] [5] [6] [7] Telemedicine has emerged dramatically during the COVID-19 pandemic and allowed clinicians to offer the standard of care to their patients with COVID-19, but with heightened public health consciousness.

Telemedicine offers an immediate virtual patient-provider visit without increasing the risk of COVID-19 exposure to patients, healthcare workers, and the public. Telemedicine also helps to preserve the supply of personal protective equipment (PPE) by limiting the number of times providers need to don PPE to clinically evaluate patients. 8 Regulatory and financial burdens to the spread of telemedicine have been lifted temporarily in light of the COVID-19 pandemic. [9] [10] [11] In a national survey of US transplant centers, 98.4% limited in-person outpatient visits for solid organ transplant recipients and 96.8% implemented telemedicine in response to the pandemic. 12 These adopted telemedicine initiatives leverage existing, underutilized telecommunications technology and nationally mandated electronic medical records. 13 Herein we present three kidney transplant recipients with COVID-19 that were managed using telemedicine via synchronous video visits integrated with an electronic medical records system, from home to inpatient settings.

A 53-year-old male with a prior history of end-stage renal disease (ESRD) secondary to hypertensive nephrosclerosis who underwent a living related kidney transplant in January 2012. He had induction therapy with rabbit antithymocyte globulin (rATG) and was maintained on an immunosuppression regimen of prednisone 2.5 mg once daily and tacrolimus dosed to achieve target trough level of 4-6 ng/ml. He was off mycophenolate mofetil (MMF) due to a history of BK viremia and skin cancer. He had stable allograft function with a baseline creatinine of 1.3 mg/dl. He called the transplant team complaining of dry cough, low-grade fever, chills, nausea and vomiting, watery diarrhea, and loss of the sense of smell. COVID-19 testing was performed in a designated drive-through area at our center on the same day (naso/oropharyngeal swab, nucleic acid test [NAT] was used to detect COVID-19 RNA by polymerase chain reaction [PCR]). He was asked to self-quarantine while awaiting his test results, according to Centers for Disease Control and Prevention (CDC) guidelines. 14 On the following day, the COVID-19 test resulted as positive, and an immediate telemedicine video visit was conducted by a transplant nephrologist. During this virtual visit, the patient was found to have worsening shortness of breath and increased work of breathing. His home vital signs were notable for blood pressure (BP) of 130/82 mmHg, heart rate of 88 beats per minute, oxygen saturation (O2 sat) of 94% on room air using a patient home kit. Given stable vital signs but increased work of breathing, the decision was made to arrange for direct hospital admission to a dedicated COVID-19 inpatient unit, avoiding the emergency room (ER) route to reduce risk of exposure to patients, health care workers, and the public. A multidisciplinary team approach was initiated, including transplant infectious disease and nephrology, hospital medicine, and admission office. The infection control office provided special instructions to the patient facilitating safe transfer for hospital admission. His laboratory findings during hospitalization are summarized in Table 1 . He was started on ceftriaxone 1 gm IV daily and azithromycin 500 mg P.O daily (to treat potential bacterial superinfection) and hydroxychloroquine 400 mg P.O twice daily for one day, then 400 mg daily on days 2, 3, 4 and 5. His electrocardiogram (ECG) showed QTc interval of 0.43 seconds. On day 3 of admission, he developed hypoxia and required 3 liters of oxygen via nasal cannula; other vitals remained within normal limits. Chest CT scan findings were consistent with features for COVID-19 infection. Azithromycin was replaced with doxycycline for concern of azithromycin induced diarrhea. His oxygen requirements gradually improved and eventually he was weaned off supplemental oxygen. On day 6 of admission, his symptoms resolved, and he was discharged home in stable condition with instructions to self-quarantine. During his hospital stay, he was followed by the transplant nephrology consult team via telemedicine video visits to reduce exposure risk and preserve PPE.

Similarly, after discharge he was followed via telemedicine video visits. His COVID-19 related hospital course and treatment are summarized in Table 2 .

A 56-year-old female with a prior history of ESRD secondary to focal segmental glomerulosclerosis who underwent a living unrelated kidney transplant in June 2019. She had induction therapy with rATG and maintained on an immunosuppression regimen of prednisone 5 mg once daily, tacrolimus dosed to achieve target trough level of 5-8 ng/ml and MMF 500 mg twice daily. She had stable allograft function with a baseline creatinine of 0.9 mg/dl. She called the transplant team complaining of dry cough, rhinorrhea, and chest tightness. The patient was asked to stop MMF. COVID-19 testing was done as mentioned in patient 1. On the following day, her COVID-19 test returned as positive, and an immediate telemedicine video visit was conducted by a transplant nephrologist. During this virtual visit, she was found to have mild symptoms and home vital signs were noted to be normal. Therefore, she was asked to continue self-quarantine and closely monitor her symptoms. On day five of the presentation, she reported not feeling well with fever of 100.7 o F and diarrhea. It was decided to proceed with a direct inpatient admission with a similar multidisciplinary approach mentioned in patient 1. On admission, her BP was 109/63 mmHg, temperature was elevated at 101 o F, heart rate was 94 beats per minute and her O2 sat was 99% on room air. Her laboratory findings during hospitalization are summarized in Table 1 .

She was started on cefepime 1 gm IV every 8 hours (to treat potential urinary tract infection), and hydroxychloroquine 400 mg P.O twice daily for one day, then 400 mg daily on days 2, 3, 4, and 5. Her ECG showed QTc interval was 0.407 seconds. On the 4 th day of admission, she developed hypoxia and required 4 liters of oxygen via nasal cannula; other vitals remained stable. A chest X-ray showed leftsided lower lobe patchy opacity. She was treated with IV tocilizumab 4 mg/Kg per dose for two doses on days 4 and 5 of admission. Her oxygen requirements gradually improved and eventually she was weaned off supplemental oxygen. On the 7 th day of admission, her symptoms resolved, and she was discharged home in stable condition with instructions to self-quarantine. During her hospitalization, she was followed by the transplant nephrology consult team via telemedicine video visits, as mentioned in patient 1. Similarly, after discharge, she was followed via telemedicine video visits. Her COVID-19 related hospital course and treatment are summarized in Table 2 . The patient had a family gathering with her extended family members and more than 20 family members were present. Several family members had mild symptoms with loss of smell and taste, and her husband had a low-grade fever. She called the transplant team complaining of mild headache, rhinorrhea, and fatigue. COVID-19 testing was done, as mentioned in patient 1. On the following day, her COVID-19 test resulted as positive and an immediate telemedicine video visit was conducted by a transplant nephrologist. During this virtual visit, she was found to have mild headache and no other symptoms. She reported home vital signs which were noted to be normal. Thus, she was asked to continue to self-quarantine and closely monitor her symptoms. Her symptoms were improving gradually without specific treatment. She was followed as an outpatient by a transplant nephrologist via telemedicine video visits and a transplant coordinator via telephone calls. Her COVID-19 related outpatient course is summarized in Table 2 .

In these cases of kidney transplant recipients who presented with COVID-19 symptoms, telemedicine provided a safe, and convenient approach to managing these patients in both home and inpatient settings. We found that telemedicine provided an immediate virtual face-to-face, patient-provider visit for clinical assessment, planning for COVID-19 testing, and safe management to reduce the risk of exposure. This approach allows for the rapid identification of those in need of hospitalization through an ER admission or an arranged direct admission, versus those who are able to remain home with selfquarantine and careful surveillance as summarized in Figure 1 and Table 3 . Also, it facilitates uninterrupted follow-up care for patients during inpatient admission and outpatient monitoring. It is worth noting that the three patients expressed good experience and satisfaction.

Our management of these patients is consistent with the emerging approach at other US transplant centers. Based on a recent national survey, nearly all in-person outpatient visits were suspended in response to the COIVD-19 crisis. Meanwhile, for those who would have been seen in an outpatient visit, telemedicine has emerged as the preferred option available to them. 12 This adoption of telemedicine on a national scale has been supported by the Centers for Medicare & Medicaid Services (CMS). Under the CMS 1135 Coronavirus waivers, Medicare will pay for office, hospital, and other visits furnished via telemedicine across the country. 9 Likewise, many states have issued licensure waiver with respect to telemedicine for out-of-state medical licensees. 10 Unlike immunocompetent patients, immunosuppressed patients may shed COVID-19 for longer periods of time, potentially increasing transmissibility. [15] [16] [17] This underscores the importance of telemedicine visits in reducing exposures from patients who have recovered from symptoms but might have persistently positive NAT tests. In our case reports, two patients who had follow-up COVID-19 tests remained positive at 18 and 21 days from onset of diagnosis. One converted to be negative at 24 and 28 days, whereas the other one was persistently positive by NAT testing at 24, 28, 35, and 42 days although she had a negative test at 38 days, and eventually converted to be negative at 45 and 48 days. While there is limited information about the duration of viral shedding for immunosuppressed patients and it

is not yet known whether protracted persistent NAT positivity reflects continued capacity for viral transmission, our case reports suggest longer periods of self-quarantine are appropriate for kidney transplant patients with 19 For patients with scheduled visits/tests that cannot be performed through telemedicine and that will occur within 6 weeks of symptom onset, patients may undergo COVID-19 repeat test-based strategy as outpatients (Table 3) .

A key strength of telemedicine was the promptness and safety in the handling of these three patients with COVID-19. Patients called in with symptoms of COVID-19, a NAT test rapidly confirmed that they were positive for COIVD-19, a telemedicine video visit was implemented, and a management plan was executed, all within 24 hours. Another important strength of telemedicine is the maintenance of continuity of care for transplant patients. Creating a systematic telemedicine schedule with the transplant clinician provides an expanded opportunity for patient questions, transmission of information, reassurance, and creating a sense that they are being cared for in a comprehensive way.

This application of telemedicine should be generalizable to other solid organ transplant recipients. By extension, telemedicine may help increase access to live kidney donor transplant evaluation, especially for those who have financial challenges to come for an in-person visit or those who live a significant distance from a transplant center. 20-22 That said, we recognize the potential limitations of telemedicine.

Access to a smart device or computer may not be available for every patient to connect via telemedicine video visits, although audio telephone visits are another option if video technology is not available. 23

Other barriers to telemedicine include out of state medical license requirements, reimbursement policies variations, and infrastructure support and personnel staffing need. 24 As such, cost-effectiveness and future reimbursements for telemedicine beyond the COVID-19 crisis remain not well defined.

In these three reports of kidney transplant recipients, telemedicine helped assess, diagnose, triage, and treat patients with COVID-19 while avoiding an ER or outpatient clinic visit. Our experience emphasizes the opportunities of telemedicine in the safe management of kidney transplant patients with COVID-19 from home to inpatient settings and in the maintenance of uninterrupted follow-up care for such immunosuppressed patients with prolonged viral shedding. Telemedicine may help increase access to care for kidney transplant recipients during and beyond the pandemic. Yet in order to increase the widespread implementation of telemedicine, existing regulatory and financial barriers should be removed permanently. Research studies to advance the practice of telemedicine and assess its effectiveness in the care kidney transplant recipients are needed.

Author Contributions: Dr. Al Ammary had full access to all the data in the case reports and takes responsibility for the integrity of the data.

Study concept and design: Al Ammary, Abuzeineh. Drafting of the manuscript: Al Ammary, Abuzeineh, Muzaale, Avery, Crews, Segev. Critical revision of the manuscript for important intellectual content: Al Ammary, Abuzeineh, Muzaale, Avery, Brennan, Brotman, Segev. Study supervision: Al Ammary.

The authors declare no conflicts of interest.

Financial Disclosure Statement: The authors declare no funding was received for this study.

The datasets generated and/or analyzed during the current study are not publicly available due to patient privacy but are available from the corresponding author on reasonable request.

Funding: This work did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. During hospitalization, patient developed shortness of breath and hypoxia. 1 Patient 2: dry cough, chest tightness, and rhinorrhea, and subsequently developed high-grade fever and diarrhea. During hospitalization, patient developed shortness of breath and hypoxia. 1 Patient 3: mild headache, rhinorrhea and fatigue; symptoms were improving gradually without specific treatment. 2 Naso-oropharyngeal swab, nucleic acid test (NAT) was use to detect COVID-19 RNA by polymerase chain reaction (PCR): (+) COVID-19 RNA detected, (−) COVID-19 RNA not detected. 3 Hydroxychloroquine 400 mg twice daily for 1 st day, then 400 mg once daily for days 2, 3, 4, and 5. 4 Tocilizumab 4 mg/kg per dose once daily for a total of two doses. ⁵Patient was also followed by a transplant coordinator via telephone calls twice weekly. 

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If You Are Sick

Virological assessment of hospitalized patients with COVID-2019

had mild acute kidney injury (AKI) and acute hyponatremia on admission

mmol/L and serum osmolarity was 258 mosm/Kg suggestive of volume depletion. Hence, his home lisinopril was stopped, and he received ringers lactate intravenous (IV) fluid replacement carefully. Figure 1: Practical workflow process for COVID-19 test and surveillance. ¹Severe shortness of breath, hypoxia, hypotension, acute chest pain

To call 911 for a transfer to hospital emergency room

Telemedicine via a synchronous video visit for clinical assessment and management

To self-quarantine per CDC guidelines and to keep home log of vital signs twice daily in the first two weeks. Patients are instructed to seek immediate medical attention if symptoms worsening

To be followed-up by a transplant coordinator via telephone calls twice weekly and transplant nephrologist via telemedicine video visits close to two-week post COVID-19 diagnosis and thereafter as clinically determined. ⁵Hospitalization through an ER admission or an arranged direct admission to COVID-19 inpatient unit. ⁶To repeat COVID-19 NAT at two-week post COVID-19 diagnosis for twice weekly until

nucleic acid test (NAT) to detect COVID-19 RNA by polymerase chain reaction (PCR)



