Abstract

Objectives: Data are so far limited on outcomes of kidney transplant recipients with COVID-19 seen at public sector hospitals in developing countries with limited resources.
Materials and Methods: We retrospectively investigated a cohort of 157 kidney transplant recipients (75% living and 25% deceased donors) seen at a public sector transplant hospital in India from March to December 2020 who had reverse-transcriptase polymerase chain reaction tests that confirmed COVID-19. Demographic data, immunosuppression regimens, clinical profiles, treatments, and outcomes were analyzed. In our center, maintenance immunosuppression was reduced according to disease severity and case-by-case evaluations. There were also 53 patients with asymptomatic or mild COVID-19 symptoms who received home care to optimize the utilization of scarce resources during travel restrictions.
Results: In our kidney transplant recipient group, median age was 43 years (133 male; 24 female patients); recipients presented at a median of 4 years after transplant. The most common comorbidities included arterial hypertension (73%) and diabetes (24%); presenting symptoms at the time of COVID-19 positivity included cough (49%), fever (58%), and sputum production (32%). Clinical severity ranged from asymptomatic (4%), mild (45%), moderate (31%), and severe (20%) disease. Statistically significant risk factors for mortality included older age, dyspnea, severe disease, obesity, allograft dysfunction prior to COVID-19, acute kidney injury, higher levels of inflammatory markers (C-reactive protein, interleukin 6, procalcitonin), abnormality in chest radiography, and intensive care/ventilator requirements (P < .05). Overall patient mortality was 9.5% (15/157) in hospitalized patients, 21% (15/71) in patients in the intensive care unit, 100% (15/15) in patients who required ventilation, and 0% among those in home treatment.
Conclusions: The mortality rate in kidney transplant recipients with COVID-19 was higher than in the nonimmunosuppressed general population (1.2%) in India. To our knowledge, this is a largest single-center study of kidney transplant recipients with COVID-19 so far.

Key words : Immunosuppression, Mortality, Severe acute respiratory syndrome coronavirus 2, Viral infection and infectious agents

Introduction

Globally, as of July 23, 2021, there have been about 192 million confirmed cases of COVID-19, including over 4 million deaths, reported to World Health Organization. As of July 24, 2021, a total of 3 646 968 156 vaccine doses have been administered.¹ The COVID-19 pandemic has already become the largest pandemic ever witnessed. India holds the second place for disease burden, with more than 15 million cumulative COVID-19 cases, death rate of 1.2% (n = 182 553), active infection rate of 13.8% (n = 2 157 538), and rate of discharged cases of 85% (n = 13 276 039).² In India, over 13 million doses of COVID-19 vaccinations have been administered, resulting in 1.3% of the population fully vaccinated and 8% who have received at least 1 dose of vaccine. However, as of April 2021, new cases of COVID-19 continue to be reported in India, with states like Maharashtra, Delhi, Kerala, and Karnataka being worse affected. On April 21, 2021, India recorded the highest 1-day total of new COVID-19 cases (n = 314 835) anywhere in the world and the country’s highest number of deaths over 24 hours.²

The COVID-19 pandemic has had a great impact on organ transplantation, as health care services are being diverted from transplant care to care for COVID-19 patients. Transplant activities have been reduced across the world, with low numbers of deceased donor transplant procedures (where available). In addition, physical attendance at outpatient clinics has been kept to a minimum, with extensive use of telemedicine and virtual clinics. Living donor transplant procedures have been restricted to the sickest patients with strict regulation, resulting in a drastic decline in the number of transplant procedures.^3-24

In India, according to the Global Observatory on Donation and Transplantation, 12 666 organ transplants, with 9751 kidney transplants, were conducted in 2019.²⁵ India holds the second position both in the number of COVID-19 cases and transplant volume.^1,2 During the COVID-19 pandemic, transplant activities have been adversely affected globally, with COVID-19 posing additional complexities, adding to the burden especially in developing nations. With transplant activities halted in many transplant centers, the numbers are expected to be considerably lower this year. Data on COVID-19 in transplant recipients are still emerging.^3-24 Recent systemic reviews have shown high mortality rates in kidney transplant recipients (KTRs) with COVID-19 during the early posttransplant period.^10,11 With regard to developing countries, literature on the course of COVID-19 and outcomes in transplant patients is especially sparse. There are limited data on the safety of continuing transplant activity, outcomes of COVID-19 in the early posttransplant period, and outcomes of transplants in donors and recipients who have recovered from COVID-19 in developing regions of the world.^23,24 In addition, public sector hospitals have been worse affected by COVID-19 versus effects shown in private sector hospitals. This study aimed to address this knowledge gap. To the best of our knowledge, this is the largest single-center experience of COVID-19 in KTRs from the largest public sector transplant hospital in India and in developing nations.

Materials and Methods

Study design and settings
This retrospective cohort study included 157 hospitalized KTRs with severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) reverse-transcriptase polymerase chain reaction (RT-PCR)-confirmed COVID-19 who were seen at a single center (Institute of Kidney Disease and Research Centre, Dr H.L. Trivedi Institute of Transplantation Sciences [IKDRC-ITS], Ahmedabad, Gujarat, India). Patients were seen from March 2020 to April 2021. During this period, 225 KTRs with COVID-19 received care from our transplant team: 157 were hospitalized and 43 were managed at home during the first wave (March to December 2020), with so far 15 patients hospitalized and 10 treated at home during the second wave (from March 2021 onward).

Hospital setting
The IKDRC-ITS is the largest public sector transplant hospital in India, with an active high-volume transplant program. From January 1997 to March 2020, 5838 kidney transplants were completed, including 943 deceased donor, 4895 living donor, and 440 living related donor paired donor transplants. As a result of the COVID-19 surge in Ahmedabad, Gujarat, India, transplant activity was suspended, per the government advisory, from March to June 2020. Specifically, living donor kidney transplant was suspended on March 18, 2020, and restarted on July 10, 2020, and deceased donor kidney transplant was suspended on March 15, 2020, and restarted on June 3, 2020. During November to December 2020, kidney transplants were reduced, leading to only 5 kidney transplants in November 2020 due to a COVID-19 surge. All transplants were suspended again on April 1, 2021, due to the ongoing second COVID-19 wave. Our transplant hospital was converted to a dedicated COVID-19 center and has remained so during the first and second wave, with 200 of 400 beds dedicated to COVID-19 cases. For patients with COVID-19 and kidney disease, there are 25 dedicated beds, which have been reserved from July 4, 2020, to November 16, 2020, and also from January to March 2021.

Definitions in the context of the study
Kidney transplant recipients were tested for COVID-19 if they exhibited COVID-19 symptoms, such as fever, cough, and dyspnea. A diagnosis of COVID-19 was confirmed by SARS-CoV-2 RT-PCR from nasal and oropharyngeal swabs. Only confirmed cases were included in our analyses; probable and suspected cases were not included. Patients were classified as having mild COVID-19 if symptoms of upper respiratory tract were mild without evidence of pneumonia or hypoxia. Patients were classified as having moderate COVID-19 if they had signs and symptoms of pneumonia, such as difficulty in breathing, hypoxia with oxygen saturation from 90% to 94% on room air, and/or respiratory rates of 24 to 30 breaths/min. Patients were classified as having severe COVID-19 if they had symptoms like tachypnea with respiratory rates of >30 breaths/min and oxygen saturation level of <90% on room air.²⁶

Early COVID-19 was determined as a patient diagnosed within 1 month of transplant surgery. Acute kidney injury (AKI) was defined as per the Kidney Disease Improving Global Outcomes (KDIGO) consensus for AKI; so far, there is no clear guideline to define AKI in the transplant population. Patients with chronic graft dysfunction were those with baseline serum creatinine above 1.5 mg/dL.

Institutional protocol for COVID-19 treatment
COVID-19-specific treatment algorithms were created by a hospital-based multidisciplinary team, and the treatment protocol was updated regularly with available evidence and resources.27-32 However, there was no standard consensus on the treatment of COVID-19. Patients in the intensive care unit were managed by the transplant teams, infectious disease consultants, and intensivists. All treatments were given as per the government guidelines for COVID-19.27-32 Investigational therapies used were favipiravir (mild to moderate cases) and remdesivir, COVID-19 convalescent plasma, tocilizumab, and intravenous immunoglobin (moderate to severe cases). All of these therapies were used as per availability of drugs. Intravenous immunoglobin was used for recipients with high immunologic risk with immunosup­pression reduction. Treatment and immunosup­pression drugs were modified on a case-by-case basis. Discharge policies also varied; during the initial stages of the pandemic (March-May 2020), patients remained admitted until their SARS-CoV-2 RT-PCR test was negative; at later stages, a negative SARS-CoV-2 RT-PCR was not mandatory for discharge. The provision of psychological, social, and rehabilitation support was readily made and proactively available to all KTRs, their families, and the health care workers to increase long-term outcomes. This included telemedicine and teleconsultation, especially if there was an added stress of traveling to and from the hospital, a door-to-door delivery of drugs, and regular counseling and updates.

Immunosuppressive regimen for kidney transplant recipients with COVID-19
The mainstay of treatment was reduction in maintenance immunosuppression according to disease severity, with case-by-case evaluations. Steroid use was increased in patients with moderate and severe disease, and no change was made in asymptomatic patients or those with mild disease. Mycophenolate or azathioprine was reduced or stopped in patients with mild disease and discontinued in those with moderate or severe disease. Calcineurin inhibitors (CNI), or sirolimus/everolimus, were discontinued in patients with severe disease, reduced in patients with moderate disease, and not changed in asymptomatic patients and those with mild disease or in home treatment.

We followed the National Organ and Tissue Transplant Organization (NOTTO), Government of India, transplant-specific guidelines for preparation of donors and recipients for transplant surgery.²²

All transplant recipients and donors signed a fully documented written informed consent form, in which they accepted the potential risk of COVID-19 infection during hospital stay and after transplant. We ensured adequate availability of personal protective equipment, training of health care workers on COVID-19, and a COVID-19 safe transplant pathway to reduce the risk of transmission. We performed routine clinical and epidemiological screening for COVID-19 using RT-PCR tests in donors and recipients. Chest computed tomography scans were performed 24 to 72 hours before surgery for all living and deceased donors. We ensured social distancing and COVID-19 preventive measures before transplant for living donors, recipients, and health care workers. We used induction and other immunosuppressive drugs based on the recipient’s own immune risk stratification as practiced before COVID-19 infection.

Data collection
The demographic characteristics and the clinical profiles of KTRs with confirmed COVID-19 were recorded from medical records, and the laboratory results were retrieved electronically from the hospital database. Laboratory parameters assessed during the study along with routine blood tests included levels of interleukin, high-sensitive C-reactive protein, lactate dehydrogenase, ferritin, D dimer, and procalcitonin. Inflammatory marker tests were done on the basis of severity of COVID-19; missing values are also reported to eliminate bias.

Ethical statement
The study was approved by the ethical committee of IKDRC-ITS. All kidney transplant procedures were done per local laws and regulations (Transplant Human Organ Act, India). We also abided by the Declaration of Helsinki and Declaration of Istanbul principles. Written informed consent was obtained from all the recipients and/or their relatives. Benefits and risks of all investigational therapies were explained.

Statistical analyses
Categorical data are expressed as number and percentage, and continuous data are expressed as median and interquartile range. To compare survivors and nonsurvivors, the Mann-Whitney test, chi-square test, Kruskal-Wallis test, and Fisher test were used as appropriate. Statistical analysis was performed using the Statistical Package for Social Science version 17.0 (SPSS Inc). P < .05 was considered statistically significant.

Results

Table 1 presents the timeline of the COVID-19 events in our study. Our study cohort included 225 KTRs with COVID-19: 172 recipients (76.4%) were hospitalized and 53 recipients (23.6%) with asymptomatic or mild COVID-19 received outpatient home treatment due to resource limitations and travel restrictions. Figure 1 shows patients who survived and died by month in 2020. From May to December 2020, 96 kidney transplants were performed (31 deceased donor and 65 living donor); COVID-19 was detected in 10 KTRs with 1 death and no graft losses, corresponding to 1% mortality rate in the early posttransplant period.

Demographic characteristics
Table 2 shows the baseline demographic characteristics, comorbidities, and medications of KTRs with COVID-19 at the time of diagnosis. Among the total cohort of hospitalized patients (n = 157), the median (IQR) age at presentation was 43 years (32-50 y), with most KTRs less than 50 years old (n = 114, 73%). The median age at presentation was higher in nonsurvivors than in survivors (53 vs 42 y; P = .002). Among hospitalized KTRs with COVID-19, 133 were men (85%). Time from transplant to presentation of COVID-19 infection was >10 years in 5 nonsurvivors (34%) versus >10 years in 18 survivors (13%) (P = .047). Twenty-four patients among all patients (15%) presented within 1 year of transplant. Hypertension (41%) and diabetes (18%) were the most common causes of end-stage kidney disease. Most KTRs in our study cohort had living related-donor kidney transplant (n = 118; 75%). Of 157 study recipients, 54 (34%) had donation from a parent. Thirty-nine patients (25%) had deceased donors, 36 (23%) had spouse donors, and 16 (10%) had near related donor paired kidney exchange donors (6 parents, 8 spouses, 2 siblings). Nine had siblings (6%) and 3 (2%) had donations from extended family members such as uncle or aunt. Most patients had received antithymocyte globulin (n = 129; 82%) as induction therapy. At the time of diagnosis of COVID-19, 135 KTRs (86%) were on triple immunosuppression with prednisolone, mycophenolate, and tacrolimus being the most common combination. Most patients (n =140; 89%) had comorbid conditions, with hypertension (73%), obesity (24%), and diabetes (24%) being the most common. Sixty-eight patients (43%) had baseline chronic graft dysfunction. Obesity (53% vs 21%) and chronic graft dysfunction (80% vs 39%) were significantly higher among nonsurvivors than survivors. The presence of 2 or more comorbid conditions was associated with high mortality (93% vs 17%; P < .001).

COVID-19 symptoms
Table 3 shows symptoms and laboratory findings of KTRs with COVID-19. Among the clinical symptoms, only dyspnea on admission was statistically significant among the nonsurvivors versus survivors (87% vs 23%; P < .001). Among the total cohort, 100 KTRs (70%) had radiological evidence of COVID-19 pneumonia. Per our grading of COVID-19, almost half of KTRs had asymptomatic (n = 7; 4%) or mild (n= 71; 45%) infection, with 31% having moderate and 20% having severe COVID-19. Patients who died had either moderate or severe COVID-19, with a significant number of severe infections among nonsurvivors (87% vs 12%).

Clinical course
SARS-CoV-2 exposure was frequently related to local community transmission (n = 41), family clustering (n = 15), social clustering (n = 26), and nosocomial/health care clustering (n = 16). SARS-CoV-2 exposure was unknown in 69 recipients, and there was no donor transmission. Average time between exposure and clinical symptoms was 8 days, time between onset of symptoms to first medical visit was 3 to 5 days, and average time between the first medical visit to hospital admission was 1 to 2 days.

Inflammatory markers
Inflammatory markers were abnormal in most patients, with worse values in the nonsurvivors (Table 3). Median (IQR) markers that were significantly worse in the nonsurvivors versus survivors included white blood cell counts (per mm³: 10 000 [6500-12 000] vs 5840 [3600-7987]; P = .003), percent neutrophils (86 [75-90] vs 76 [67-84]; P = .013), percent lymphocytes (12 [8-20] vs 20 [12-27]; P = .023), procalcitonin (ng/mL: 0.96 [0.25-9.9] vs 0.11 [0.05-0.99]; P = .005), high-sensitive C-reactive protein (mg/L: 160 [87-178] vs 43 [16-85]; P < .001), ferritin (ng/mL: 996 [425-1276] vs 362 [185-994]; P = .02), D-dimer (μg/L: 2200 [1247-4865] vs 980 [490-2100]; P = .011), lactate dehydrogenase (U/L: 598 [356-1129] vs 302 [246-387]; P < .001), and interleukin 6 (pg/mL: 69 [44-135] vs 48 [31-65]; P = .015). There was no statistically significant dif­ference found in hemoglobin level, platelet counts, and alanine aminotransferase level between the 2 groups.

Treatment modalities and outcome
Table 4 shows treatment modalities and outcomes of KTRs with COVID-19. In most of the patients, immunosuppression treatment was changed according to COVID-19 severity. With regard to steroid treatment, overall 79 patients (50.3%) with moderate or severe infection and all patients in the nonsurvivor group received increased doses of steroids. Antimetabolites (mainly mycophenolate mofetil) were altered in the form of discontinuation (80%) or reduction (20%). The dose of CNI was unchanged in 58% of cases, and in 19% of cases the dose was tailored. In 23% of cases, CNI was completely stopped. Supportive care and oxygen therapy (ranging from a nasal cannula to mechanical ventilation) and adjustments in immunosuppression were the main interventions in the initial period of March to April 2020 due to resource limitations. Therapeutic measures used in the cohort included azithromycin, hydroxychloroquine, favipiravir, intravenous immunoglobulin, COVID-19 convalescent plasma, and remdesivir. Investigational therapies like tocilizumab (7%), remdesivir (47%), and COVID-19 convalescent plasma (13%) were used in moderate to severe cases. There were no major adverse events associated with any of the investigational therapies used. Overall, the mortality rate was 9.5% (15/157) in the cohort, with 1% mortality (1/96) in the early post-transplant period. Median (range) follow-up duration was 123 days (36-276 d). Half of the cases required supplemental oxygen therapy during the stay. All 15 patients (9.5%) who required mechanical ventilation had died. Of 157 hospitalized KTRs with COVID-19, 31 patients (20%) required intensive care unit care. Acute kidney injury occurred in 50% of the patients in the cohort, with need of hemodialysis in 26 patients (16%). Graft loss (n = 10, 6%) occurred in patients who already had chronic graft dysfunction before getting COVID-19.

All transplants and elective surgeries were on hold as of April 1, 2021, marking an ongoing second COVID-19 wave in Ahmedabad, Gujarat, India. Clinical severity ranged from asymptomatic (20%), mild (56%), moderate (20%), to severe (4%) in 25 KTRs during the second wave, with one mortality so far in a patient with severe disease. Of 25 patients, 10 patients with asymptomatic/mild COVID-19 infection had home treatment and 15 patients with moderate or severe disease were hospitalized.

Table 5 shows that COVID-19 mortality was higher in the first wave than in the second wave. Overall mortality was 7.1% (16/225) or 9.3% (16/172) in the hospitalized cohort and 100% in patients on mechanical ventilation. Mortality was higher in the hospitalized cohort in the first wave than in the ongoing second wave (9.5% in the first and 6.6% in the second wave). There was no mortality in the 43 KTRs with asymptomatic/mild COVID-19 who had home treatment in the first wave and in the 10 KTRs with home treatment in the second wave; 5 of these patients required hospital admission to monitor comorbid conditions. COVID-19 severity seemed to increase with older age.

Discussion

We have reported a retrospective single-center study on COVID-19-positive KTRs who were seen at a public sector transplant hospital in India. To our knowledge, this is the largest single-center KTR cohort with COVID-19 infection reported from a developing country.

Mortality in the general population versus dialysis and kidney transplant in India and the developed world
Other studies have reported on mortality in the general population and among patients after dialysis or kidney transplant in the developed world and in India.^33-38 In our cohort of hospitalized KTRs, the mortality rate was 9.5%, which is higher compared with the general population in India, possibly due to immunosuppression and associated comorbid conditions. Recent studies in Indian have reported 12% to 37% mortality of COVID-19 in dialysis patients.^35,36 The COVID-19 mortality per 1 million population is 1747 in the United States versus 129 in India as of April 19, 2021. In our study, the mortality rate among KTRs was lower than in other solid-organ transplant recipients with COVID-19 from the developed world (4.8% to 33%), possibly due to the relatively younger age of KTRs with COVID-19 in India. Table 6 shows the clinical features and outcomes of COVID-19 in organ transplant recipients. There are several differences among our cohort of patients compared with other published reports. In India, 90% of KTRs are dependent on government schemes for transplant and follow-up, and poor education and socioeconomic status may have resulted in late presentation to the hospital. It is possible that mortality could be improved if there were no resource limitations of health care workers and there were better testing and medicines available, especially in the initial months of the pandemic, where an “infodemic” seemed more lethal than the COVID-19 pandemic.³⁹

Our study also showed that KTRs with asymptomatic/mild COVID-19 can be managed at home, with favorable outcomes and 0% mortality, as described previously.⁴⁰ Therefore, home treatment can be a feasible option for KTRs with asymptomatic and or mild COVID-19 in developing regions with limited health care resources. A total of 96 patients underwent kidney transplants from May to December 2020, and 10 KTRs were confirmed by RT-PCR to have COVID-19; there was 1 death, resulting in mortality of 1% in our center. The mortality rate in patients with chronic kidney disease on maintenance dialysis hospitalized with COVID-19 in our public-sector hospital was 37.9% (22/58) from May 2020 to July 2020 (unpublished data). Our study findings support that kidney transplant should be continued with careful selection of donors and recipients, and this should be as per the NOTTO transplant-specific guidelines with respect to COVID-19.²⁷ This information helped in counseling candidates on wait lists for decision of transplant in our center. Results from our study can add to further amendments of the consensus guide­lines for transplant during the COVID-19 pandemic.

The clinical features among our cohort were similar to previous reports in transplant settings and similar to those found in the general population (Table 6).^10-22 In a previous study,⁴¹ blood group A was associated with more COVID-19 cases; our cohort showed blood group O as the most common in COVID-19, with no preference with regard to any particular blood group. In most of the cases, AKI developed, with need for renal replacement in several patients. No graft biopsies were performed due to logistic issues.

Immune modulation and therapeutics in COVID-19
Modification of immunosuppression as per severity of COVID-19 is tricky but is the most important aspect in management of COVID-19 in transplant recipients. The imbalance can result in risk of rejection or worsening of COVID-19 disease. The institutional protocol for immunosuppression modulation was to stop or reduce antimetabolites in all positive cases and decrease or stop CNI in moderate to severe cases. Patients were advised to gradually increase immunosuppressive doses after 14 days of discharge in a step-wise manner. This approach was quite successful in our cohort.

During the early period of the COVID-19 pandemic (from April 15 to May 8, 2020), 2149 health care professionals, who were low-risk individuals, reported mild COVID-19 with diverse long-term symptoms, which disrupted work, social, and home life.⁴² In a retrospective cohort study using electronic health records from 236 379 survivors of COVID-19, evidence showed substantial neurological and psychiatric morbidity in the 6 months after COVID-19 infection. Risks were greatest in, but not limited to, patients who had severe COVID-19.⁴³ We did not observe substantial neurological and psychiatric morbidity in our cohort with the early proactive provision of psychological and social support and rehabilitation as recently reported.⁴⁴

The repercussions of the pandemic and those related to possible additional waves are uncertain and unpredictable.^45,46 Only the prioritization and strengthening of organ transplant programs by governments, especially in developing countries, could guarantee a return to normal.

Limitations
The study encountered certain limitations. First, the study included only a single center. Second, because of its retrospective design, a prospective study was not possible due to resource limitations and unprecedented COVID-19 surges. Third, there was wide variability of treatment protocols used throughout the study, which was expected as no definitive therapy was available. It is possible that our data showed an underreporting of COVID-19 in transplant recipients as patients were treated at home with teleconsultation for mild febrile illness. Our report focused only on kidney transplants, and thus conclusions may not be broadly applicable to other organ transplant recipients. Detailed demographic and laboratory analyses were not included for KTRs with COVID-19 who had home treatment during the ongoing second wave due to resource limitations.

Conclusions

In 225 KTRs with COVID-19 who were seen at a public sector transplant hospital in India, outcomes were acceptable. To our knowledge, this is a largest single-center study so far from India. Our data provided relevant insights into management and outcomes of KTRs with COVID-19 in India and may thus serve to improve outcomes of KTRs with COVID-19 in the ongoing second wave with better preparedness and understanding of COVID-19. The mortality rates in KTR with COVID-19 (7.1% overall, 9.3% in the hospitalized cohort, 100% on mechanical ventilation) were higher compared with the nonim­munosuppressed general population (1.2%) but lower compared with the developed world.

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