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COVID-19 and kidney disease: Progress in health inequity from low income settings

      Abstract

      COVID-19 pandemic has had significant impact on the incidence and prevalence of acute kidney injury (AKI) and chronic kidney disease (CKD) globally and in low-income settings. CKD increases the risk of developing COVID-19 and COVID-19 causes AKI directly or indirectly and its associated with high mortality in severe cases. Outcomes of COVID-19 associated kidney disease were not equitable globally due to lack of health infrastructure, challenges in diagnostic testing and management of COVID-19 in low-income settings. COVID-19 also significantly impacted kidney transplant rates and mortality among kidney transplant recipients. Vaccine availability and uptake remains a significant challenge in low- and lower-middle income countries (LLMICs) as compared to high income countries.
      In this review, we explore the inequities in LLMICs and attempt to highlight the progress made in the prevention, diagnosis and management of patients with COVID-19 and kidney disease. We recommend further studies into the challenges, lessons learnt and progress made in the diagnosis, management and treatment of patients with COVID-19 related kidney diseases and suggest ways to improve the care and management of patients with COVID-19 and kidney disease.

      Keywords

      Introduction

      Severe Acute Respiratory Syndrome Corona Virus 2 (SARS-CoV-2) causing Corona Virus Disease - 2019 (COVID-19) has had significant impact on the burden and management of patients with kidney diseases globally and in low- and lower-middle income countries (LLMICs) [
      • Alessandri F
      • Pistolesi V
      • Manganelli C
      • Ruberto F
      • Ceccarelli G
      • Morabito S
      • et al.
      Acute Kidney Injury and COVID-19: A Picture from an Intensive Care Unit.
      ,
      • Carlson N
      • Nelveg-Kristensen KE
      • Freese Ballegaard E
      • Feldt-Rasmussen B
      • Hornum M
      • Kamper AL
      • et al.
      Increased vulnerability to COVID-19 in chronic kidney disease.
      ,
      • Cheng Y
      • Luo R
      • Wang K
      • Zhang M
      • Wang Z
      • Dong L
      • et al.
      Kidney disease is associated with in-hospital death of patients with COVID-19.
      ,
      • Henry BM
      • Lippi G.
      Chronic kidney disease is associated with severe coronavirus disease 2019 (COVID-19) infection.
      ,
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ]. COVID-19 increases the risk of proteinuria, haematuria, tubulopathies, acute kidney injury (AKI) and chronic kidney disease (CKD) [
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ,
      • Velez JCQ
      • Caza T
      • Larsen CP.
      COVAN is the new HIVAN: the re-emergence of collapsing glomerulopathy with COVID-19.
      ,
      • Peleg Y
      • Kudose S
      • D'Agati V
      • Siddall E
      • Ahmad S
      • Nickolas T
      • et al.
      Acute kidney injury due to collapsing glomerulopathy following COVID-19 infection.
      ] and its associated with severe COVID-19 disease [
      • Carlson N
      • Nelveg-Kristensen KE
      • Freese Ballegaard E
      • Feldt-Rasmussen B
      • Hornum M
      • Kamper AL
      • et al.
      Increased vulnerability to COVID-19 in chronic kidney disease.
      ,
      • Henry BM
      • Lippi G.
      Chronic kidney disease is associated with severe coronavirus disease 2019 (COVID-19) infection.
      ,
      • D'Marco L
      • Puchades MJ
      • Romero-Parra M
      • Gimenez-Civera E
      • Soler MJ
      • Ortiz A
      • et al.
      Coronavirus disease 2019 in chronic kidney disease.
      ]. COVID-19 infection when complicated by AKI or in patients with underlying CKD or kidney failure are associated with increased mortality especially in low-income settings [
      • Cheng Y
      • Luo R
      • Wang K
      • Zhang M
      • Wang Z
      • Dong L
      • et al.
      Kidney disease is associated with in-hospital death of patients with COVID-19.
      ,
      • Adapa S
      • Aeddula NR
      • Konala VM
      • Chenna A
      • Naramala S
      • Madhira BR
      • et al.
      COVID-19 and renal failure: challenges in the delivery of renal replacement therapy.
      ,
      • Blumenthal D
      • Fowler EJ
      • Abrams M
      • Collins SR.
      Covid-19—implications for the health care system.
      ,
      • Bong C-L
      • Brasher C
      • Chikumba E
      • McDougall R
      • Mellin-Olsen J
      • Enright A.
      The COVID-19 pandemic: effects on low-and middle-income countries.
      ,
      • Diana NE
      • Kalla IS
      • Wearne N
      • Kariv S
      • Davidson B
      • Rusch J
      • et al.
      Acute kidney injury during the COVID-19 pandemic–experience from two tertiary centres in South Africa.
      ]. The care and management of patients on kidney replacement therapy (KRT) was also significantly affected by the COVID-19 pandemic leading to missing dialysis sessions. Transplant programs were suspended with uncertainties in immunosuppression dosing among some kidney transplant recipients (KTR) associated with increased morbidity and mortality [
      • Achilonu OJ
      • Fabian J
      • Musenge E.
      Modeling Long-Term Graft Survival With Time-Varying Covariate Effects: An Application to a Single Kidney Transplant Centre in Johannesburg, South Africa.
      ,
      • Craig-Schapiro R
      • Salinas T
      • Lubetzky M
      • Abel BT
      • Sultan S
      • Lee JR
      COVID-19 outcomes in patients waitlisted for kidney transplantation and kidney transplant recipients.
      ,
      • Godara S
      • Saraf KK
      • Sadasukhi T
      • Gupta H
      • Gupta M
      • Sadasukhi N
      • et al.
      COVID-19 infection in kidney transplant recipients: A single centre study from Northern India.
      ,
      • Hadi YB
      • Naqvi SF
      • Kupec JT
      • Sofka S
      • Sarwari A.
      Outcomes of COVID-19 in solid organ transplant recipients: a propensity-matched analysis of a large research network.
      ,
      • Hilbrands LB
      • Duivenvoorden R
      • Vart P
      • Franssen CF
      • Hemmelder MH
      • Jager KJ
      • et al.
      COVID-19-related mortality in kidney transplant and dialysis patients: results of the ERACODA collaboration.
      ].
      The diagnosis and management of patients with COVID-19 associated kidney disease has been greatly affected as a result of the COVID-19 pandemic [
      • Aylward R
      • Bieber B
      • Guedes M
      • Pisoni R
      • Tannor EK
      • Dreyer G
      • et al.
      The Global Impact of the COVID-19 Pandemic on In-Center Hemodialysis Services: An ISN-Dialysis Outcomes Practice Patterns Study Survey.
      ,
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ]. Inequitable distribution of resources needed for the screening, diagnosis and optimal management of COVID-19 associated kidney disease has been highlighted coupled with the looming vaccine inequity in LLMICs though high vaccine rollout was the most effective remedy for the prevention of COVID-19 transmission and decrease in COVID-19 severity [
      • Hou Y-C
      • Lu K-C
      • Kuo K-L.
      The efficacy of COVID-19 vaccines in chronic kidney disease and kidney transplantation patients: a narrative review.
      ,
      • Asundi A
      • O'Leary C
      • Bhadelia N
      Global COVID-19 vaccine inequity: The scope, the impact, and the challenges.
      ,
      • Choi EM.
      COVID-19 vaccines for low-and middle-income countries.
      ].
      In this review, we set out to describe the impact of COVID-19 on kidney disease and the progress made in the care and management of patients with COVID-19 associated kidney disease and provide suggestions to improve the diagnosis and management of COVID-19 associated kidney disease in LLMICs.

      COVID-19 and kidney disease

      COVID-19 affects multiple organs including the kidneys. The effect of COVID-19 on the kidneys ranges from asymptomatic proteinuria, haematuria to acute kidney injury (AKI) and progression to chronic kidney disease (CKD) and kidney failure [
      • Alessandri F
      • Pistolesi V
      • Manganelli C
      • Ruberto F
      • Ceccarelli G
      • Morabito S
      • et al.
      Acute Kidney Injury and COVID-19: A Picture from an Intensive Care Unit.
      ,
      • Carlson N
      • Nelveg-Kristensen KE
      • Freese Ballegaard E
      • Feldt-Rasmussen B
      • Hornum M
      • Kamper AL
      • et al.
      Increased vulnerability to COVID-19 in chronic kidney disease.
      ,
      • Cheng Y
      • Luo R
      • Wang K
      • Zhang M
      • Wang Z
      • Dong L
      • et al.
      Kidney disease is associated with in-hospital death of patients with COVID-19.
      ,
      • Henry BM
      • Lippi G.
      Chronic kidney disease is associated with severe coronavirus disease 2019 (COVID-19) infection.
      ,
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ]. Kidney failure in those with underlying CKD and severe cases of AKI in patients with severe COVID-19 may require KRT [
      • Adapa S
      • Aeddula NR
      • Konala VM
      • Chenna A
      • Naramala S
      • Madhira BR
      • et al.
      COVID-19 and renal failure: challenges in the delivery of renal replacement therapy.
      ]. SARS-CoV-2 can have direct or indirect effect on the kidneys. Directly, it can cause AKI by cytokine storm, angiotensin 2 pathway activation, dysregulation of the complement system, hypercoagulability, microangiopathy and collapsing glomerulopathy [
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ,
      • Velez JCQ
      • Caza T
      • Larsen CP.
      COVAN is the new HIVAN: the re-emergence of collapsing glomerulopathy with COVID-19.
      ,
      • Peleg Y
      • Kudose S
      • D'Agati V
      • Siddall E
      • Ahmad S
      • Nickolas T
      • et al.
      Acute kidney injury due to collapsing glomerulopathy following COVID-19 infection.
      ]. Indirectly, COVID-19 increases the risk of AKI through hemodynamic instability, hypoxemia, sepsis and exposure to nephrotoxins [
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ]. COVID-19 may lead to CKD as a consequence of clinical or subclinical AKI or as a result of residual inflammation associated with SARS-CoV-2 infection [
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ].
      The pooled incidence of AKI was reported in a meta-analysis to be 10% (95% CI 7.0-12.0%) [
      • Xu Z
      • Tang Y
      • Huang Q
      • Fu S
      • Li X
      • Lin B
      • et al.
      Systematic review and subgroup analysis of the incidence of acute kidney injury (AKI) in patients with COVID-19.
      ] and a pooled prevalence of 17% (range 0.5% - 80.5%) among hospitalized patients with COVID-19 [
      • Valeri AM
      • Robbins-Juarez SY
      • Stevens JS
      • Ahn W
      • Rao MK
      • Radhakrishnan J
      • et al.
      Presentation and outcomes of patients with ESKD and COVID-19.
      ]. The wide variations result from varying AKI definitions, differences in gender, race, carrier status of APOL-1 risk alleles, co-morbidities, severity of COVID-19 and changes in the virulence of SARS-CoV-2 with different mutations over time [
      • Hung AM
      • Shah SC
      • Bick AG
      • Yu Z
      • Chen H-C
      • Hunt CM
      • et al.
      APOL1 risk variants, acute kidney injury, and death in participants with African ancestry hospitalized with COVID-19 from the Million Veteran Program.
      ].
      The consensus report of the 25th Acute Disease Quality Initiative (ADQI) summarized all of these risk factors for COVID-19 into three broad categories - demographic risk factors, AKI risk factors at admission and during hospitalization [
      • Nadim MK
      • Forni LG
      • Mehta RL
      • Connor MJ
      • Liu KD
      • Ostermann M
      • et al.
      COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup.
      ]. We have expanded the list of risk factors to include those relevant to low income settings[Figure 1] [
      • Alessandri F
      • Pistolesi V
      • Manganelli C
      • Ruberto F
      • Ceccarelli G
      • Morabito S
      • et al.
      Acute Kidney Injury and COVID-19: A Picture from an Intensive Care Unit.
      ,
      • Cheng Y
      • Luo R
      • Wang K
      • Zhang M
      • Wang Z
      • Dong L
      • et al.
      Kidney disease is associated with in-hospital death of patients with COVID-19.
      ,
      • Diana NE
      • Kalla IS
      • Wearne N
      • Kariv S
      • Davidson B
      • Rusch J
      • et al.
      Acute kidney injury during the COVID-19 pandemic–experience from two tertiary centres in South Africa.
      ,
      • Meena P
      • Bhargava V
      • Rana DS
      • Bhalla AK
      • Gupta A.
      COVID-19 and the kidney: A matter of concern.
      ]. Some medications are such as vancomycin, aminoglycosides and angiotensin converting enzyme inhibitor (ACEi) are also associated with AKI [
      • Pannu N
      • Nadim MK.
      An overview of drug-induced acute kidney injury.
      ,
      • See YP
      • Young BE
      • Ang LW
      • Ooi XY
      • Chan CP
      • Looi WL
      • et al.
      Risk Factors for development of acute kidney injury in COVID-19 patients: A retrospective observational cohort study.
      ]. COVID-associated AKI is associated with increased mortality especially in severe cases [
      • Diana NE
      • Kalla IS
      • Wearne N
      • Kariv S
      • Davidson B
      • Rusch J
      • et al.
      Acute kidney injury during the COVID-19 pandemic–experience from two tertiary centres in South Africa.
      ,
      • Kolhe NV
      • Fluck RJ
      • Selby NM
      • Taal MW.
      Acute kidney injury associated with COVID-19: a retrospective cohort study.
      ].
      Figure 1:
      Figure 1Risk factors for acute kidney injury in patients with COVID-19 in low income settings
      Proteinuria occurs in 24-84% of patients with COVID-19 in the presence or absence of AKI and it is a predictor of mortality with or without AKI and/or microscopic hematuria [
      • Mohamed MM
      • Velez JCQ.
      Proteinuria in COVID-19.
      ]. Proteinuria may also suggest subclinical kidney pathology or underlying comorbidities such as diabetes mellitus and/or hypertension [
      • Su H
      • Yang M
      • Wan C
      • Yi L-X
      • Tang F
      • Zhu H-Y
      • et al.
      Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China.
      ]. The first COVID-19-related glomerular disease were case reports describing collapsing glomerulopathy [
      • Velez JCQ
      • Caza T
      • Larsen CP.
      COVAN is the new HIVAN: the re-emergence of collapsing glomerulopathy with COVID-19.
      ,
      • Kissling S
      • Rotman S
      • Gerber C
      • Halfon M
      • Lamoth F
      • Comte D
      • et al.
      Collapsing glomerulopathy in a COVID-19 patient.
      ,
      • Meijers B
      • Hilbrands LB.
      The clinical characteristics of coronavirus-associated nephropathy.
      ] found mostly in Black patients who were carriers with APOL1 risk alleles presenting with nephrotic range proteinuria and AKI [
      • Hung AM
      • Shah SC
      • Bick AG
      • Yu Z
      • Chen H-C
      • Hunt CM
      • et al.
      APOL1 risk variants, acute kidney injury, and death in participants with African ancestry hospitalized with COVID-19 from the Million Veteran Program.
      ,
      • Kissling S
      • Rotman S
      • Gerber C
      • Halfon M
      • Lamoth F
      • Comte D
      • et al.
      Collapsing glomerulopathy in a COVID-19 patient.
      ]. Minimal change glomerular injury, anti-glomerular basement membrane glomerulonephritis and membranous glomerulonephritis have all been described in patients with COVID-19 disease. Sub-nephrotic proteinuria is mainly of tubular origin predominantly due to 1-α microglobulin [
      • Kudose S
      • Batal I
      • Santoriello D
      • Xu K
      • Barasch J
      • Peleg Y
      • et al.
      Kidney biopsy findings in patients with COVID-19.
      ,
      • Huart J
      • Bouquegneau A
      • Lutteri L
      • Erpicum P
      • Grosch S
      • Résimont G
      • et al.
      Proteinuria in COVID-19: prevalence, characterization and prognostic role.
      ]. Proximal tubulopathy with acute Fanconi syndrome has also been described and it is associated with severe disease. Tubulopathy has been shown to precede the onset of AKI and disappeared with kidney recovery [
      • Werion A
      • Belkhir L
      • Perrot M
      • Schmit G
      • Aydin S
      • Chen Z
      • et al.
      SARS-CoV-2 causes a specific dysfunction of the kidney proximal tubule.
      ,
      • Morelle J
      • Wérion A
      • Belkhir L
      • Chen Z
      • Jadoul M
      • Devuyst O.
      L'infection à SARS-CoV-2 cause une dysfonction tubulaire proximale du rein.
      ,
      • Kormann R
      • Jacquot A
      • Alla A
      • Corbel A
      • Koszutski M
      • Voirin P
      • et al.
      Coronavirus disease 2019: acute Fanconi syndrome precedes acute kidney injury.
      ].

      Inequity and progress in the screening and diagnosis of COVID-19

      Diagnostic polymerase chain reaction test is preferred to antigen testing for diagnosing SARS-CoV-2 infection [
      World Health Organization
      Laboratory testing of human suspected cases of novel coronavirus (nCoV) infection Interim guidance, 2019.
      ] and intensified polymerase chain reaction testing decreased the rate of transmission during the first wave [
      • Rannan-Eliya RP
      • Wijemunige N
      • Gunawardana J
      • Amarasinghe SN
      • Sivagnanam I
      • Fonseka S
      • et al.
      Increased Intensity Of PCR Testing Reduced COVID-19 Transmission Within Countries During The First Pandemic Wave: Study examines increased intensity of reverse transcription–polymerase chain reaction (PCR) testing and its impact on COVID-19 transmission.
      ]. The diagnosis and management of kidney disease at the onset of the COVID-19 pandemic was very challenging especially in LLMICs given the inability to carry out rapid polymerase chain reaction testing due to lack of resourced laboratories and technical staff [
      • Tannor EK.
      Challenges in kidney care in a lower middle income country during the COVID-19 pandemic–the Ghanaian perspective.
      ]. The International Society of Nephrology and the Dialysis Outcome and Practice Pattern (ISN-DOPPS) survey highlighted gross disparities in the testing for COVID-19 during the pandemic [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ]. Diagnostic polymerase chain reaction testing was reportedly unavailable or of limited availability in low income countries (LIC)(72%) and lower-middle income countries (LMIC) (68%) as compared to 20% in high income countries at the peak of the pandemic [
      • Tannor EK.
      Challenges in kidney care in a lower middle income country during the COVID-19 pandemic–the Ghanaian perspective.
      ]. Rates declined during the period of the ISN-DOPPS survey in November 2020 - March 2021 from 68% to 21% in LMICs but only marginally from 72% to 62% in LIC as compared to the peak of the pandemic in March 2022. The turnaround time for receiving diagnostic test results was also delayed [
      • Torres I
      • Sippy R
      • Sacoto F.
      Assessing critical gaps in COVID-19 testing capacity: the case of delayed results in Ecuador.
      ]. Same day results were received in 60% in high income country as compared to 13-21% in LLMICs according to respondents, whereby those infected had delayed diagnosis and possibility of impacting higher transmission rates. The low testing rates supported the hypothesis that rates of COVID-19 and mortality in Africa was low due to under-testing and not from a low infection rate [
      • Bamgboye EL
      • Omiye JA
      • Afolaranmi OJ
      • Davids MR
      • Tannor EK
      • Wadee S
      • et al.
      COVID-19 Pandemic: Is Africa Different?.
      ,
      • Connor A
      • Hariharan N
      • Carson S
      • Sanders KC
      • Vosburg KB
      • Sabot O.
      Access To COVID-19 Testing In Low- And Middle-Income Countries Is Still Critical To Achieving Health Equity.
      ,
      • Lone SA
      • Ahmad A.
      COVID-19 pandemic–an African perspective.
      ].
      During the peak of the pandemic, a mandatory negative test was required before discharge of patients, this criterion was later revised by the World Health Organization(WHO) on 27th May 2020, where patients were considered to have recovered after 2 weeks without symptoms. This new criterion was useful in LLMICs due to challenges with frequent testing [
      World health Organization Criteria for releasing COVID-19 patients from isolation. 17th June 2020. Scientific Brief.
      ] as the previous criteria for discharge from isolation was clinical recovery and two negative reverse transcriptase polymerase chain reaction results on sequential results taken at least 24 hours apart [
      World Health Organization
      Laboratory testing of human suspected cases of novel coronavirus (nCoV) infection Interim guidance, 2019.
      ]. These changes were recommended by the WHO based on limited laboratory supplies, equipment and personnel in low income settings.
      Testing capacity and rapid results of diagnostic tests improved through the pandemic as tests were made readily available for the diagnosis of COVID-19 by some governments. In the Philippines and Kenya, the costs for testing was between $11-55 for diagnostic testing, however, in India, Ghana and Zambia, it was free in public institutions. Even within a country, there was wide variation of costs leading to even more misinformation. Within the same country prices ranged from $0-91 in Kenya, $0-99 in Zambia, $0-104 in the Philippines and $0-14 in India depending whether facility is public or private. Stigmatization and government and/or employer enforced isolation after a positive test, which often discouraged people from availing themselves for testing even when the test was readily available [
      • Connor A
      • Hariharan N
      • Carson S
      • Sanders KC
      • Vosburg KB
      • Sabot O.
      Access To COVID-19 Testing In Low- And Middle-Income Countries Is Still Critical To Achieving Health Equity.
      ].
      Rates of COVID-19 in Africa for example were favourable in terms of infection and mortality rates as compared to the rest of the world. At the peak of the pandemic in August 2020, though Africa inhabits 17.2% of the world's population, it accounted for 5% of COVID-19 cases and 3% of COVID-19 related mortalities. Seeding effect, low testing capacity, low population density, more youthful population, exposure to previous infections and environmental conditions postulated as reasons for this phenomenon [
      • Bamgboye EL
      • Omiye JA
      • Afolaranmi OJ
      • Davids MR
      • Tannor EK
      • Wadee S
      • et al.
      COVID-19 Pandemic: Is Africa Different?.
      ]. LLMICs, however, have unique challenges due to poverty and low infrastructure leading to poor outcomes in severe cases [
      • Bong C-L
      • Brasher C
      • Chikumba E
      • McDougall R
      • Mellin-Olsen J
      • Enright A.
      The COVID-19 pandemic: effects on low-and middle-income countries.
      ,
      • Hopman J
      • Allegranzi B
      • Mehtar S.
      Managing COVID-19 in low-and middle-income countries.
      ]. The gross inequities in the screening and diagnosis of COVID-19 in kidney failure patients on haemodialysis during the COVID-19 pandemic were, however, associated with higher increased mortality [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ].

      COVID-19 and AKI in low income settings

      Generally, LLMICs have challenges in the diagnosis of AKI due to low nephrology workforce, absence of quality laboratory infrastructure and quality histopathology even during non-pandemic times [
      • Cerdá J
      • Mohan S
      • Garcia-Garcia G
      • Jha V
      • Samavedam S
      • Gowrishankar S
      • et al.
      Acute kidney injury recognition in low-and middle-income countries.
      ]. The pandemic widened the gap in care in LLMICs. Furthermore, the lack of adequate specialized medical/laboratory personnel, significant knowledge gaps among primary healthcare providers, suboptimal diagnostic capacity limited the detection and optimization in management of AKI [
      • Igiraneza G
      • Dusabejambo V
      • Finklestein FO
      • Rastegar A.
      Challenges in the recognition and management of acute kidney injury by hospitals in resource-limited settings.
      ].
      AKI occurred in 5-15% of COVID-19 patients and its associated with increased mortality of up to 90% especially in patients admitted into intensive care units (ICU) in China during the onset of the pandemic [
      • Naicker S
      • Yang C-W
      • Hwang S-J
      • Liu B-C
      • Chen J-H
      • Jha V.
      The Novel Coronavirus 2019 epidemic and kidneys.
      ]. A retrospective study in New York, however, showed 87.2% attained full recovery of kidney function in most patients with AKI in the ICU [
      • Hittesdorf E
      • Panzer O
      • Wang D
      • Stevens JS
      • Hastie J
      • Jordan DA
      • et al.
      Mortality and renal outcomes of patients with severe COVID-19 treated in a provisional intensive care unit.
      ]. A recent study in South Africa reported that AKI occurred in 33.9% of patients admitted with COVID-19 and 24.3% were admitted to ICU [
      • Diana NE
      • Kalla IS
      • Wearne N
      • Kariv S
      • Davidson B
      • Rusch J
      • et al.
      Acute kidney injury during the COVID-19 pandemic–experience from two tertiary centres in South Africa.
      ]. The risk of AKI during the pandemic was associated with severity of COVID-19, high comorbidity burden, underlying CKD, decreased vaccination rate, high risk carriers of APOL1 and decreased access to specialized care [
      • Long JD
      • Strohbehn I
      • Sawtell R
      • Bhattacharyya R
      • Sise ME.
      COVID-19 Survival and its impact on chronic kidney disease.
      ].
      Pre-renal and acute tubular necrosis were the most common causes of AKI indirectly but collapsing glomerulopathy also termed COVID-19 associated Nephropathy (COVAN) were suggested to be caused directly by SARS-CoV-2 [
      • Velez JCQ
      • Caza T
      • Larsen CP.
      COVAN is the new HIVAN: the re-emergence of collapsing glomerulopathy with COVID-19.
      ,
      • Nlandu YM
      • Makulo J-RR
      • Pakasa NM
      • Sumaili EK
      • Nkondi CN
      • Bukabau JB
      • et al.
      First case of COVID-19-associated collapsing glomerulopathy in sub-Saharan Africa.
      ]. There are also reports of pauci-immune crescentic necrotizing glomerulonephritis as a result of COVID-19 vaccination [
      • Shakoor MT
      • Birkenbach MP
      • Lynch M.
      ANCA-associated vasculitis following Pfizer-BioNTech COVID-19 vaccine.
      ]. Such diagnosis requires adequate nephropathology which may be lacking in most low-income settings. Where histopathology is available, most countries in LLMICs use light microscopy without immunofluorescence and electron microscopy [
      • Bijol V
      • Farag YM
      • Harris DC
      • Levin A
      • Roy-Chaudhury P
      • Singh AK
      • et al.
      Renal pathology practice globally: identifying needs and meeting the challenge.
      ].
      A recent introduction of the Extended Kidney Disease Improving Global Outcome (eKDIGO) AKI criteria was adopted by the International Society of Nephrology (ISN) AKI 0by25 studies for COVID-19. The new definition includes the decrement of serum creatinine of 26.5umol/L in 48 hours or fall by 1.5 times from the baseline in 7 days, which identified twice as many cases of AKI as compared to the traditional criteria (31.7% versus 16.8%) [
      • Wainstein M
      • MacDonald S
      • Fryer D
      • Young K
      • Balan V
      • Begum H
      • et al.
      Use of an extended KDIGO definition to diagnose acute kidney injury in patients with COVID-19: A multinational study using the ISARIC–WHO clinical characterisation protocol.
      ]. This classification has significant logistic challenges if implemented in LLMICs as it requires frequent measurement of serum creatinine even in stable cases, which is prohibitive due to cost.
      Optimal management of AKI in the light of COVID-19 is impossible without an adequate nephrology workforce. The nephrologists per million population (pmp) in high income countries is 28.5pmp as compared to 2.4pmp in LMIC and 0.31pmp in LICs. This is a direct result of the dearth of training programs to train both physicians and nurses. Africa has 9 of the 10 countries with the lowest nephrology workforce globally [
      • Wearne N
      • Okpechi IG
      • Swanepoel CR.
      Nephrology in South Africa: Not Yet ubuntu.
      ,
      • Osman MA
      • Alrukhaimi M
      • Ashuntantang GE
      • Bellorin-Font E
      • Gharbi MB
      • Braam B
      • et al.
      Global nephrology workforce: gaps and opportunities toward a sustainable kidney care system.
      ,
      • Sharif MU
      • Elsayed ME
      • Stack AG.
      The global nephrology workforce: emerging threats and potential solutions!.
      ]. There are also challenges in access to KRT in low income settings in Africa leading to increased mortality [
      • Naicker S.
      End-stage renal disease in sub-Saharan Africa.
      ]. There is inequity in the distribution of haemodialysis services in most countries in low income settings even within the same country [
      • Tannor E
      • Awuku Y
      • Boima V
      • Antwi S.
      The geographical distribution of dialysis services in Ghana.
      ]. Patients pay out of pocket for haemodialysis sessions in some countries and mortality increases in the absence of KRT in some low income settings.
      During the COVID-19 pandemic patients with underlying CKD or AKI with COVID-19 were prevented from accessing ICU care when needed due to perceived poor prognosis during triaging [
      • Aylward R
      • Bieber B
      • Guedes M
      • Pisoni R
      • Tannor EK
      • Dreyer G
      • et al.
      The Global Impact of the COVID-19 Pandemic on In-Center Hemodialysis Services: An ISN-Dialysis Outcomes Practice Patterns Study Survey.
      ,
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ]. This resulted in were increased mortality from treatable causes of AKI in low income settings [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ]. Though the roll-out of vaccination decreased incidence and prevalence of COVID-19 and COVID-19 associated AKI worldwide, there has not been any marked documented improvement in the access to KRT as only 7% of those on KRT live in LLMICs [
      • Harris DC
      • Davies SJ
      • Finkelstein FO
      • Jha V
      • Donner J-A
      • Abraham G
      • et al.
      Increasing access to integrated ESKD care as part of universal health coverage.
      ].
      Some suggested solutions to improve diagnosis of AKI include engaging local and regional stakeholders in healthcare financing, developing educational programs and guidelines, training of healthcare workers, providing adequate health care resources, linking with regional health care projects and improving research opportunities in low income settings [
      • Lunyera J
      • Kilonzo K
      • Lewington A
      • Yeates K
      • Finkelstein FO.
      Acute kidney injury in low-resource settings: barriers to diagnosis, awareness, and treatment and strategies to overcome these barriers.
      ].

      COVID-19 and chronic kidney disease in low-income settings

      CKD increases the risk of AKI and AKI can lead to CKD and progression to kidney failure in both hospitalized and non-hospitalized patients with COVID-19 [
      • Chawla LS
      • Eggers PW
      • Star RA
      • Kimmel PL.
      Acute kidney injury and chronic kidney disease as interconnected syndromes.
      ,
      • Bowe B
      • Xie Y
      • Xu E
      • Al-Aly Z.
      Kidney outcomes in long COVID.
      ]. COVID-19 infection could be due to the presence of unknown underlying CKD before hospitalization [
      • Cheng Y
      • Zhang N
      • Luo R
      • Zhang M
      • Wang Z
      • Dong L
      • et al.
      Risk Factors and Outcomes of Acute Kidney Injury in Critically Ill Patients with Coronavirus Disease 2019.
      ]. There is a high global prevalence of CKD of 11% [
      • Coresh J
      • Astor BC
      • Greene T
      • Eknoyan G
      • Levey AS.
      Prevalence of chronic kidney disease and decreased kidney function in the adult US population: Third National Health and Nutrition Examination Survey.
      ] which is even higher in low income continents such as Africa with a prevalence of 13.9-15.8% [
      • Stanifer JW
      • Jing B
      • Tolan S
      • Helmke N
      • Mukerjee R
      • Naicker S
      • et al.
      The epidemiology of chronic kidney disease in sub-Saharan Africa: a systematic review and meta-analysis.
      ,
      • Stanifer JW
      • Muiru A
      • Jafar TH
      • Patel UD.
      Chronic kidney disease in low-and middle-income countries.
      ,
      • Kaze AD
      • Ilori T
      • Jaar BG
      • Echouffo-Tcheugui JB.
      Burden of chronic kidney disease on the African continent: a systematic review and meta-analysis.
      ].
      COVID-19 survivors may also develop long-term kidney issues [
      • Bowe B
      • Xie Y
      • Xu E
      • Al-Aly Z.
      Kidney outcomes in long COVID.
      ]. A Chinese study reported a 35% reduction in estimated glomerular filtration rate (eGFR) six months after COVID-19 hospitalization [
      • Cheng Y
      • Zhang N
      • Luo R
      • Zhang M
      • Wang Z
      • Dong L
      • et al.
      Risk Factors and Outcomes of Acute Kidney Injury in Critically Ill Patients with Coronavirus Disease 2019.
      ]. Even without documented evidence of AKI on admission, 13% of patients showed a reduction in eGFR during follow-up [
      • Huang C
      • Huang L
      • Wang Y
      • Li X
      • Ren L
      • Gu X
      • et al.
      6-month consequences of COVID-19 in patients discharged from hospital: a cohort study.
      ]. Although many patients have normalization of creatinine after AKI, the kidneys may not recover completely and increase the risk of CKD over time [
      • Chawla LS
      • Eggers PW
      • Star RA
      • Kimmel PL.
      Acute kidney injury and chronic kidney disease as interconnected syndromes.
      ]. Progression of kidney disease in COVID-19 is likely multifactorial and could be driven by continuous inflammation, intrinsic tubular lesions or improper repair [
      • Bowe B
      • Xie Y
      • Xu E
      • Al-Aly Z.
      Kidney outcomes in long COVID.
      ]. In most patients with CKD in low income countries, progression to kidney failure requiring dialysis increases mortality due to absence of KRT and increased cost associated with poor outcomes [
      • Tannor E
      • Awuku Y
      • Boima V
      • Antwi S.
      The geographical distribution of dialysis services in Ghana.
      ,
      • Ashuntantang G
      • Osafo C
      • Olowu WA
      • Arogundade F
      • Niang A
      • Porter J
      • et al.
      Outcomes in adults and children with end-stage kidney disease requiring dialysis in sub-Saharan Africa: a systematic review.
      ]. The risk factors associated with worse outcome with CKD include increasing age, diabetes mellitus, hypertension, the unavailability of adequate nephrology workforce and the absence of adequate diagnostic tools [
      • D'Marco L
      • Puchades MJ
      • Romero-Parra M
      • Gimenez-Civera E
      • Soler MJ
      • Ortiz A
      • et al.
      Coronavirus disease 2019 in chronic kidney disease.
      ].

      Awareness of CKD in low income settings

      There has not been much progress made in raising awareness for the prevention and management of risk factors for COVID-19-associated kidney disease in low income settings. Moreover, incidence and prevalence of the non-communicable diseases such as diabetes and hypertension that can lead to kidney disease are also increasing and account for 80% of global deaths in LLMICs [
      • Alwan A
      • MacLean DR.
      A review of non-communicable disease in low-and middle-income countries.
      ]. Governments must invest more in health to decrease burden of NCDs and conditions that impact kidney health. Public health interventions such as education, healthy dietary lifestyle, and exercise should be part of a national agenda to prevent CKD. There has been poor governmental support in this regard with few sustainable programs to decrease the burden of kidney disease. Such public health interventions have been championed by individuals and some non-governmental organizations (NGOs) such as the World Kidney Day activities of the ISN [
      • Tannor EK
      • Calice-Silva V.
      Kidney health for all-Efforts in low-income settings to enhance community engagement, kidney health awareness and screening.
      ,
      • Kumela Goro K
      • Desalegn Wolide A
      • Kerga Dibaba F
      • Gashe Fufa F
      • Wakjira Garedow A
      • Edilu Tufa B
      • et al.
      Patient Awareness, Prevalence, and Risk Factors of Chronic Kidney Disease among Diabetes Mellitus and Hypertensive Patients at Jimma University Medical Center, Ethiopia.
      ,
      • Oluyombo R
      • Ayodele O
      • Akinwusi P
      • Okunola O
      • Gbadegesin B
      • Soje M
      • et al.
      Awareness, knowledge and perception of chronic kidney disease in a rural community of South‑West Nigeria.
      ]. Such initiatives should be encouraged to decrease the kidney disease burden with or without COVID-19. The reduction of the burden of kidney disease in patients with COVID-19 is based on the decrease in the transmission of SARS-CoV-2. This calls for optimization of vaccination across the globe with the early detection and appropriate management of cases to prevent AKI and CKD [
      • Wijewickrama E
      • Bajpai D
      • Hafidz M
      • Robinson B
      • Johnson D
      • Liew A
      • et al.
      Availability and prioritization of covid-19 vaccines among patients with chronic kidney disease and kidney transplant-a global survey by the international society of nephrology.
      ].

      Inequity in kidney failure patients on chronic haemodialysis with COVID-19 in low income settings

      Patients on chronic dialysis are at increased risk of COVID-19 due to decreased immune status, frequent hospital visits for haemodialysis sessions, difficulty in maintaining social distancing during haemodialysis session especially in constrained spaces among dialysis units from low income settings [
      • Adapa S
      • Aeddula NR
      • Konala VM
      • Chenna A
      • Naramala S
      • Madhira BR
      • et al.
      COVID-19 and renal failure: challenges in the delivery of renal replacement therapy.
      ,
      • Hilbrands LB
      • Duivenvoorden R
      • Vart P
      • Franssen CF
      • Hemmelder MH
      • Jager KJ
      • et al.
      COVID-19-related mortality in kidney transplant and dialysis patients: results of the ERACODA collaboration.
      ,
      • Weinhandl ED
      • Wetmore JB
      • Peng Y
      • Liu J
      • Gilbertson DT
      • Johansen KL.
      Initial Effects of COVID-19 on Patients with ESKD.
      ,
      • Combe C
      • Kirsch AH
      • Alfano G
      • Luyckx VA
      • Shroff R
      • Kanbay M
      • et al.
      At least 156 reasons to prioritize COVID-19 vaccination in patients receiving in-centre haemodialysis.
      ]. The incidence of SARS-CoV-2 infection range from 1-19.9% in dialysis populations and had significant mortality of 10-41% [
      • Hilbrands LB
      • Duivenvoorden R
      • Vart P
      • Franssen CF
      • Hemmelder MH
      • Jager KJ
      • et al.
      COVID-19-related mortality in kidney transplant and dialysis patients: results of the ERACODA collaboration.
      ,
      • Valeri AM
      • Robbins-Juarez SY
      • Stevens JS
      • Ahn W
      • Rao MK
      • Radhakrishnan J
      • et al.
      Presentation and outcomes of patients with ESKD and COVID-19.
      ,
      • Jager KJ
      • Kramer A
      • Chesnaye NC
      • Couchoud C
      • Sánchez-Álvarez JE
      • Garneata L
      • et al.
      Results from the ERA-EDTA Registry indicate a high mortality due to COVID-19 in dialysis patients and kidney transplant recipients across Europe.
      ,
      • Scarpioni R
      • Manini A
      • Valsania T
      • De Amicis S
      • Albertazzi V
      • Melfa L
      • et al.
      Covid-19 and its impact on nephropathic patients: the experience at Ospedale “Guglielmo da Saliceto” in Piacenza.
      ,
      • Alberici F
      • Delbarba E
      • Manenti C
      • Econimo L
      • Valerio F
      • Pola A
      • et al.
      A report from the Brescia Renal COVID Task Force on the clinical characteristics and short-term outcome of hemodialysis patients with SARS-CoV-2 infection.
      ,
      • De Meester J
      • De Bacquer D
      • Naesens M
      • Meijers B
      Couttenye MM, De Vriese AS. Incidence, characteristics, and outcome of COVID-19 in adults on kidney replacement therapy: a regionwide registry study.
      ,
      • Robinson BM
      • Guedes M
      • Alghonaim M
      • Cases A
      • Dasgupta I
      • Gan L
      • et al.
      Worldwide Early Impact of COVID-19 on Dialysis Patients and Staff and Lessons Learned: A DOPPS Roundtable Discussion.
      ]. In the peak of the pandemic due to lockdown measures it was reported that patients in low income countries missed their dialysis sessions more frequently than those in high income countries. According to the ISN-DOPPS survey, haemodialysis sessions were reportedly missed in 66-67% in LLMICs as compared to 20-33% in upper-middle income countries and high income countries [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ]. Transportation to and from haemodialysis units were reportedly more affected in patients in those in LLMICs. These, however, improved with easing of lockdown restrictions anecdotally but published evidence is lacking.
      There were also major supply chain disruptions of haemodialysis consumables in low income countries during the pandemic. Intensive care admission, mechanical ventilation and dialysis during hospitalization were more restricted or prohibited in patients with kidney failure on chronic dialysis in low income settings as compared to high income settings during the peak of the pandemic (Figure 2) [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ].
      Figure 2
      Figure 2Medical interventions such as ICU admission, mechanical ventilation and dialysis while hospitalized became more restricted or prohibited for chronic dialysis patients admitted to the hospital with COVID-19 by World Bank income
      [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ]
      Patients with kidney failure were at increased risk of infection due to frequent centre visits for haemodialysis sessions. They are also particularly at risk due to the decrease in the immunity as a result of the kidney failure. Close proximity by patients during transportation as well as long durations in close proximity during haemodialysis sessions further increased their risk [
      • Combe C
      • Kirsch AH
      • Alfano G
      • Luyckx VA
      • Shroff R
      • Kanbay M
      • et al.
      At least 156 reasons to prioritize COVID-19 vaccination in patients receiving in-centre haemodialysis.
      ].
      Guidelines were instituted by many societies [
      • Basile C
      • Combe C
      • Pizzarelli F
      • Covic A
      • Davenport A
      • Kanbay M
      • et al.
      Recommendations for the prevention, mitigation and containment of the emerging SARS-CoV-2 (COVID-19) pandemic in haemodialysis centres.
      ,
      Centre for Disease Control and Prevention
      Interim additional guidance for infection prevention and control for patients with suspected or confirmed COVID-19 in nursing homes.
      ,
      • Elsayed HM
      • Wadee S
      • Zaki MS
      • Were AJ
      • Ashuntantang GE
      • Bamgboye EL
      • et al.
      Guidelines for the prevention, detection and management of the renal complications of COVID-19 in Africa.
      ,
      National Institute of Health and Care Excellence
      COVID-19 rapid guideline: managing COVID-19.
      ] to help decrease the spread of infections in haemodialysis units but this could not be strictly adhered to in most low income settings due to poor testing and unavailability of resources for transmission prevention. Some dialysis centres were reportedly turning away dyspneic patients for fear of COVID-19 transmission to other patients as testing was not readily available but this improved when testing was made more readily available. The rollout of vaccinations in patients with kidney failure on dialysis was also filled with challenges with uptake due to various myths about the vaccines but vaccine hesitancy has improved with time based on better education [
      • Tannor EK.
      Challenges in kidney care in a lower middle income country during the COVID-19 pandemic–the Ghanaian perspective.
      ,
      • Mwai P.
      2021 Covid-19 vaccines: Why some African states can't use their vaccines'.
      ].
      Health workers worked under poor conditions and were exposed to infections due to absence of the required personal protective equipment. Diagnostic polymerase chain reaction and rapid antigen test were not readily available for asymptomatic and symptomatic testing of staff in most low income setting when required [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ,
      • Scohy A
      • Anantharajah A
      • Bodéus M
      • Kabamba-Mukadi B
      • Verroken A
      • Rodriguez-Villalobos H.
      Low performance of rapid antigen detection test as frontline testing for COVID-19 diagnosis.
      ]. Staff in haemodialysis units in low income settings were tested infrequently when asymptomatic 11-14% as compared to 28% in high income countries [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ] which lead to stress, psychological problems and stigmatization among healthcare workers [
      • Bagcchi S.
      Stigma during the COVID-19 pandemic.
      ,
      • Uvais NA
      • Aziz F
      • Hafeeq B.
      COVID-19-related stigma and perceived stress among dialysis staff.
      ].

      COVID-19 and kidney transplantation

      The rapid evolution of the COVID-19 pandemic had a two-fold effect on kidney transplant recipients (KTR) and programs. On one hand, KTR are more vulnerable to severe COVID-19-related morbidity and mortality [
      • Caillard S
      • Anglicheau D
      • Matignon M
      • Durrbach A
      • Greze C
      • Frimat L.
      On behalf of the French SOT COVID registry. An initial report from the French SOT COVID registry suggests high mortality due to Covid− 19 in recipients of kidney transplants.
      ,
      • Pereira M
      • Mohan S
      • Cohen D.
      COVID-19 in solid organ transplant recipients: Initial report from the US epicenter.
      ,
      • Fernández-Ruiz M
      • Andrés A
      • Loinaz C
      • Delgado JF
      • López-Medrano F
      • San Juan R
      • et al.
      COVID-19 in solid organ transplant recipients: a single-center case series from Spain.
      ], while on the other, there is a decline in the transplant capacity and volume for the need for more ethical distribution of scarce resources [
      • Emanuel JE
      • Persad G
      Upshur R: original: Fair Allocation of Scarce Medical Resources in the Time of Covid-19.
      ,
      • Aubert O
      • Yoo D
      • Zielinski D
      • Cozzi E
      • Cardillo M
      • Dürr M
      • et al.
      COVID-19 pandemic and worldwide organ transplantation: a population-based study.
      ]. The pandemic exposed the pre-existing inequities and healthcare deficiencies in healthcare worldwide [
      • Paremoer L
      • Nandi S
      • Serag H
      • Baum F
      Covid-19 pandemic and the social determinants of health.
      ], but countries with lower resources suffered to a greater extent [
      • Tannor E
      • Bieber B
      • Shah D
      • Phiri C
      • Evans R
      • Aylward R
      • et al.
      COVID-19 pandemic highlights global inequities in chronic hemodialysis care: A dopps/isn survey.
      ].

      Clinical outcomes of COVID-19 in kidney transplant recipients

      The presence of medical comorbidities (eg. hypertension, diabetes, cardiovascular diseases) in KTRs makes it difficult to assess the attributable impact of transplantation on morbidity and mortality. The mortality due to COVID-19 remains high in KTRs even after adjustment for co-morbidities [
      • Caillard S
      • Anglicheau D
      • Matignon M
      • Durrbach A
      • Greze C
      • Frimat L.
      On behalf of the French SOT COVID registry. An initial report from the French SOT COVID registry suggests high mortality due to Covid− 19 in recipients of kidney transplants.
      ,
      • Pereira M
      • Mohan S
      • Cohen D.
      COVID-19 in solid organ transplant recipients: Initial report from the US epicenter.
      ,
      • Fernández-Ruiz M
      • Andrés A
      • Loinaz C
      • Delgado JF
      • López-Medrano F
      • San Juan R
      • et al.
      COVID-19 in solid organ transplant recipients: a single-center case series from Spain.
      ,
      • Roberts MB
      • Izzy S
      • Tahir Z
      • Al Jarrah A
      • Fishman JA
      • El Khoury J.
      COVID-19 in solid organ transplant recipients: dynamics of disease progression and inflammatory markers in ICU and non-ICU admitted patients.
      ]. In a systematic review of 74 studies (between March 2020 to January 2021) including 5559 KTRs with COVID-19, the mortality was 23% (95% CI: 21% - 27%) which remained high after adjustment of age, sex and comorbidities [
      • Sargazi M
      • Shenkin A
      • Roberts NB.
      Aluminium-induced injury to kidney proximal tubular cells: Effects on markers of oxidative damage.
      ]. However, on comparing 2307 KTR with 231,047 non-transplant controls who were propensity-matched for age and comorbidities in a multi-center study, there was no difference in the rates of mortality, although transplant recipients had higher rates of hospitalization and AKI [
      • Sargazi M
      • Shenkin A
      • Roberts NB.
      Aluminium-induced injury to kidney proximal tubular cells: Effects on markers of oxidative damage.
      ].
      The effect of immunosuppression on clinical outcomes of COVID-19 remains obscure. The harmful impact of COVID-19 is a result of the complex interplay of direct viral injury and the host's immune response with evidence that dysregulated and intense immune responses cause severe disease [
      • Chen G
      • Wu D
      • Guo W
      • Cao Y
      • Huang D
      • Wang H
      • et al.
      Clinical and immunologic features in severe and moderate coronavirus disease 2019.
      ]. Since immunosuppressive drugs modulate host responses the intensity or type of immunosuppression can potentially affect the severity of COVID-19. The adjustment of immunosuppression in KTRs with COVID-19 is complex and needs to be tailored according to disease activity and risk of graft rejection. Lymphopenia which is a risk factor for severe COVID-19 can be potentiated by antimetabolites which are recommended to be discontinued. Calcineurin inhibitors (CNIs) are usually continued as they inhibit interleukin-6 and interleukin-1 which is instrumental in causing dysregulated immune response leading to severe COVID-19. Specific drugs like mammalian target of rapamycin (mTOR) inhibitors have some biological activity against SARS-COV-2 but this needs further evaluation [
      • Conti P
      • Ronconi G
      • Caraffa A
      • Gallenga C
      • Ross R
      • Frydas I
      Induction of pro-inflammatory cytokines (IL-1 and IL-6) and lung inflammation by Coronavirus-19 (COVI-19 or SARS-CoV-2): anti-inflammatory strategies.
      ]. Other strategies for the management of COVID-19 remain similar to the general population. Remdesivir is reported to be safe in KTR [
      • Elec F
      • Magnusson J
      • Elec A
      • Muntean A
      • Antal O
      • Moisoiu T
      • et al.
      COVID-19 and kidney transplantation: the impact of remdesivir on renal function and outcome-a retrospective cohort study.
      ,
      • Thakare S
      • Gandhi C
      • Modi T
      • Bose S
      • Deb S
      • Saxena N
      • et al.
      Safety of remdesivir in patients with acute kidney injury or CKD.
      ].
      As compared with non-transplant populations, KTRs are at a higher risk of COVID-19 associated AKI (50% risk, 95 %CI: 44%-56% in a systematic review of 74 studies involving 5559 KTRs) even after adjustment for comorbidities [
      • Sargazi M
      • Shenkin A
      • Roberts NB.
      Aluminium-induced injury to kidney proximal tubular cells: Effects on markers of oxidative damage.
      ]. This can adversely affect long-term graft outcomes. In a multi-center, prospective study from India evaluating KTRs with COVID-19 associated AKI, complete graft recovery at 3 months was seen in 40.5% of patients, with high rates of proteinuria (47%) and graft failure (14.3%) [
      • Bajpai D
      • Deb S
      • Bose S
      • Gandhi C
      • Modi T
      • Katyal A
      • et al.
      Recovery of kidney function after AKI because of COVID-19 in kidney transplant recipients.
      ]. This underscores the kidney involvement in long COVID-19 syndromes and the need for long-term close monitoring in this high-risk population.

      Evidence on clinical outcomes from low-resource settings

      Evidence is scarce on the clinical outcomes of COVID-19 with kidney disease from low resource settings. In a systematic review of 74 studies published from March 2020 to January 2021, 86% of studies were from North America and Europe, while 14% were from Asia /Pacific and none from Latin America and Africa [
      • Sargazi M
      • Shenkin A
      • Roberts NB.
      Aluminium-induced injury to kidney proximal tubular cells: Effects on markers of oxidative damage.
      ]. They reported lower mortality rates in the USA (estimated proportion of deaths: 18%; 95% CI: 14%–23%) than in Asia/Pacific, but this difference was not statistically significant [
      • Sargazi M
      • Shenkin A
      • Roberts NB.
      Aluminium-induced injury to kidney proximal tubular cells: Effects on markers of oxidative damage.
      ]. Initial reports from India documented higher mortality rates (27% -30%) in KTRs as compared to the general population with 100% mortality in ventilated patients [
      • Godara S
      • Saraf KK
      • Sadasukhi T
      • Gupta H
      • Gupta M
      • Sadasukhi N
      • et al.
      COVID-19 infection in kidney transplant recipients: A single centre study from Northern India.
      ,
      • Jasuja S
      • Sagar G
      • Bahl A
      • Verma S.
      COVID-19 Infection Clinical Profile, Management, Outcome, and Antibody Response in Kidney Transplant Recipients: A Single Centre Experience.
      ]. A multi-center cohort of 250 KTRs with COVID-19 from India reported 10% mortality which is lower than that reported in high-income countries [
      • Kute VB
      • Bhalla AK
      • Guleria S
      • Ray DS
      • Bahadur MM
      • Shingare A
      • et al.
      Clinical profile and outcome of COVID-19 in 250 kidney transplant recipients: a multicenter cohort study from India.
      ]. The largest reported cohort from Southeast Asia is 259 KTRs which demonstrated a change in the clinical spectrum of COVID-19 over subsequent pandemic waves [
      • Kute VB
      • Meshram HS
      • Navadiya VV
      • Chauhan S
      • Patel DD
      • Desai SN
      • et al.
      Consequences of the first and second COVID-19 wave on kidney transplant recipients at a large Indian transplant centre.
      ]. Improvement in clinical outcomes after the first wave of pandemic can be attributable to advances in health care infrastructure and the success of vaccination programs, with India for example having over a 1 billion individuals vaccinated by 15th May 2022. In a head-to-head comparison by propensity score-matched cohort from India, there was no difference in mortality amongst solid organ transplant recipients with COVID-19 as compared to non-transplant patients [
      • Kute VB
      • Meshram HS
      • Chauhan S
      • Patel H
      • Banerjee S
      • Desai S
      • et al.
      A Propensity-Matched Analysis of COVID-19 in Kidney Transplant Recipients Compared With Non-Kidney Transplant Patients: A Single-Center Report From India.
      ].
      In a narrative review evaluating 6 studies from Latin America, mortality from COVID-19 in KTRs ranged from 14.3% to 35.4%; and from 25.5% to 40.9% in KTRs hospitalized with COVID-19 [
      • Cristelli MP
      • Viana LA
      • Tedesco-Silva H
      • Medina-Pestana J.
      COVID-19 Among Kidney Transplant Recipients: A Look Into Latin America.
      ]. Similarly, a report from South Africa documented 20% mortality in KTRs [
      • Jones ES
      • Davidson BJ
      • Barday Z
      • Barday Z
      • Davids MR
      • Thomson D
      • et al.
      COVID-19 and the kidney: a South African state healthcare experience.
      ].
      Another malady that struck LLMICs (especially in Southeast Asia) was COVID-19-associated mucormycosis [
      • Muthu V
      • Agarwal R
      • Patel A
      • Kathirvel S
      • Abraham OC
      • Aggarwal AN
      • et al.
      Definition, diagnosis, and management of COVID-19-associated pulmonary mucormycosis: Delphi consensus statement from the Fungal Infection Study Forum and Academy of Pulmonary Sciences, India.
      ]. In the largest multicenter cohort of COVID-19-associated mucormycosis in KTRs (61 KTRs from 18 centers) the incidence of COVID-19-associated mucormycosis was 4.4% and the mortality rate was 26.2% [
      • Meshram HS
      • Kute VB
      • Yadav DK
      • Godara S
      • Dalal S
      • Guleria S
      • et al.
      Impact of COVID-19-associated Mucormycosis in Kidney Transplant Recipients: A Multicenter Cohort Study.
      ]. The emergence of such opportunistic infections can further strain the already overwhelmed healthcare resources. Thus, there is a need for a high level of preparedness for timely diagnosis and management of such emerging infections during the pandemic.

      Development of management guidelines from low middle-income countries

      COVID-19 pandemic was marked by the exponential growth of misinformation, alarming misbeliefs against emerging therapies, and dilemmas in decision making that hindered healthcare delivery. In India, the National Organ and Tissue Transplant Organization (NOTTO), the apex body governing transplantation published guidelines on transplant-specific issues on COVID-19 early in the pandemic [
      • Kute V
      • Guleria S
      • Prakash J
      • Shroff S
      • Prasad N
      • Agarwal SK
      • et al.
      NOTTO transplant specific guidelines with reference to COVID-19.
      ]. Indian society of organ transplantation (ISOT) and Latin America formulated local guidelines on transplantation in donors and recipients recovering from COVID-19 [
      • Kute VB
      • Guleria S
      • Bhalla AK
      • Sharma A
      • Agarwal SK
      • Sahay M
      • et al.
      ISOT consensus statement for the kidney transplant recipient and living donor with a previous diagnosis of COVID-19.
      ,
      • Millán DAC
      • Fajardo-Cediel W
      • Tobar-Roa V
      • García-Perdomo HA
      • Autrán-Gómez AM.
      Strategies to Mitigate the Impact of COVID 19 Pandemic on Organ Donation and Kidney Transplantation in Latin America.
      ].

      Collateral damage to transplant program development

      According to the Global Observatory on Organ Donation and Transplantation, all regions of the world suffered a decrease in transplant volume [
      • Kute VB
      • Meshram HS
      • Mahillo B
      • Dominguez-Gil B
      Transplantation in India and China during the COVID-19 pandemic.
      ]. However, there was a stark difference in the speed with which the high income countries could re-build their transplant volume maintaining their total number of transplants per year, unlike the LLMICs [
      • Aubert O
      • Yoo D
      • Zielinski D
      • Cozzi E
      • Cardillo M
      • Dürr M
      • et al.
      COVID-19 pandemic and worldwide organ transplantation: a population-based study.
      ]. In Latin America in the year 2020 for instance, there was a 32% - 64% reduction in the number of transplants, which was significantly higher than the global average of 16% in high income countries [
      • Aubert O
      • Yoo D
      • Zielinski D
      • Cozzi E
      • Cardillo M
      • Dürr M
      • et al.
      COVID-19 pandemic and worldwide organ transplantation: a population-based study.
      ]. The worst hit was the deceased donor program, which is already in its nascent stages in the developing world [
      • Kute VB
      • Tullius SG
      • Rane H
      • Chauhan S
      • Mishra V
      • Meshram HS.
      Global Impact of the COVID-19 Pandemic on Solid Organ Transplant.
      ].
      A multicenter study from India reported a dramatic impact on transplant programs in general, however, the centers in the public sector were more affected as compared to private institutions [
      • Meshram HS
      • Kute VB
      • Swarnalatha G
      • Hegde U
      • Sharma A
      • Sahay M
      • et al.
      Effect of Coronavirus Disease 2019 on Transplantation and Nephrology in India: A Nationwide Report From India.
      ]. Most of these centers were converted into dedicated COVID-19 centers which was the need of the hour. Thus, regulatory policies, healthcare capacity, state of SARS-CoV-2 transmission, and public awareness governed this collateral damage. The long-term sequelae of delaying transplantation is still unclear. Limited evidence suggests that the risk of hospitalization and mortality associated with COVID-19 is higher in patients on the waitlist as compared to KTRs [
      • Craig-Schapiro R
      • Salinas T
      • Lubetzky M
      • Abel BT
      • Sultan S
      • Lee JR
      COVID-19 outcomes in patients waitlisted for kidney transplantation and kidney transplant recipients.
      ]. Studies from India have documented favorable outcomes and stressed the importance of continuing elective transplant procedures amid the pandemic if the healthcare facilities are not overwhelmed [
      • Soin AS
      • Choudhary NS
      • Yadav SK
      • Saigal S
      • Saraf N
      • Rastogi A
      • et al.
      Restructuring living-donor liver transplantation at a high-volume center during the COVID-19 pandemic.
      ,
      • Singhal A
      • Sahota GS
      • Srivastava P
      • Makki K
      • Agarwal A
      • Khan AA
      • et al.
      Living donor liver transplantation during the COVID-19 pandemic:“elective” but “necessary”.
      ]. Furthermore, a study from India reported a serendipitous silver lining of reduced infections in liver transplants performed amid the pandemic due to health policy changes to control SARS-CoV-2 spread [
      • Menon J
      • Hakeem AR
      • Rammohan A
      • Sundaramoorthy S
      • Kanagavelu RG
      • Reddy MS
      • et al.
      Living Donor Liver Transplantation During the COVID-19 Pandemic: A Serendipitous Silver Lining!.
      ]. This is especially vital for transplant programs from the LLMICs where infections are the primary cause of death with a functioning graft. The pandemic taught the need for concerted efforts at a global level to facilitate improved pandemic preparedness so that transplant programs can be sustainable even in pandemics.

      COVID-19 vaccine equity

      Vaccination against SARS-COV-2 remains the cornerstone of preventing severe COVID-19 infection and its complications among individuals with kidney disease despite the decreased antibody responses observed among these patients compared to general population [
      • Hou Y-C
      • Lu K-C
      • Kuo K-L.
      The efficacy of COVID-19 vaccines in chronic kidney disease and kidney transplantation patients: a narrative review.
      ,
      • Glenn DA
      • Hegde A
      • Kotzen E
      • Walter EB
      • Kshirsagar AV
      • Falk R
      • et al.
      Systematic review of safety and efficacy of COVID-19 vaccines in patients with kidney disease.
      ]. In order to maximize the benefits of COVID-19 vaccines globally, they should be produced in adequate amounts, made affordable, distributed equitably so that they are available where needed, and deployed effectively at the individual, country and regional level. This is challenging, especially in the LLMICs of Asia, Africa and Latin America.
      Low income setting were significantly disadvantaged in the vaccine roll out [
      • Akinbodewa AA
      • Adejumo OA.
      Awareness and Practice of Vaccination of Chronic Hemodialysis Patients by Specialist Nephrology Practitioners in Nigeria: A Cross-Sectional Survey.
      ]. While some countries such as United Arab Emirates have 99% of their citizens having received one dose of vaccine as at 11th May 2022, LMICs like Ghana and Nigeria have 30.5% and 13% respectively [
      • Connor Alison
      • H N.
      • Carson Sarah
      • et al.
      Access to COVID-19 testing in low- and middle-income countries is still critical to achieving health equity.
      ]. While high income countries and upper-middle income countries have 74.9-77.9% of their population fully vaccinated, LLMICs have 14.7 – 54.4% of their population fully vaccinated as at 4th June 2022 (Figure 3) [
      • Hannah Ritchie E.M.
      • Rodés-Guirao Lucas
      • Appel Cameron
      • Giattino Charlie
      • Ortiz-Ospina Esteban
      • Hasell Joe
      • Macdonald Bobbie
      • Beltekian Diana
      • Roser Max
      Coronavirus (COVID-19) vaccinations 2022.
      ]. There was a modest improvement in vaccine rollout but this is far from optimal. It was suggested that vaccine equity is necessary to win the war on COVID-19 and patients on chronic dialysis should be prioritized [
      • Combe C
      • Kirsch AH
      • Alfano G
      • Luyckx VA
      • Shroff R
      • Kanbay M
      • et al.
      At least 156 reasons to prioritize COVID-19 vaccination in patients receiving in-centre haemodialysis.
      ]. LLMICs do not have the same ability to purchase vaccines, do not have the technology and capacity to produce their own vaccines and lack the infrastructure to deploy these vaccines efficiently. This has led to large disparities in COVID-19 vaccination especially among those with kidney disease between high and low-income countries in the world.
      Figure 3
      Figure 3Showing the number of people fully vaccinated per world bank income status
      [
      • Emanuel EJ
      • Luna F
      • Schaefer GO
      • Tan K-C
      • Wolff J.
      Enhancing the WHO's proposed framework for distributing COVID-19 vaccines among countries.
      ]
      The COVID Vaccine Global Access (COVAX) facility was created by the WHO in April 2021 in order to facilitate the access of COVID-19 vaccines to both high and low-income countries equally [
      • Emanuel EJ
      • Luna F
      • Schaefer GO
      • Tan K-C
      • Wolff J.
      Enhancing the WHO's proposed framework for distributing COVID-19 vaccines among countries.
      ]. The key elements of this program are that vaccination should proceed in stages, and priority given to high-risk individuals before proceeding to vaccinate the others in the general population. All participating countries would initially receive a stock of vaccines sufficient to vaccinate 20% of the population. COVAX was helpful in initiating the COVID vaccination programs, especially in some LLMIC countries, by being able to procure and provide vaccines at affordable prices. However, the amounts of vaccines provided through COVAX were inadequate to meet the demand, resulting in most of the high income countries leaving the program and purchasing vaccines directly from the manufacturers. This has resulted in vaccines developed in USA and Europe becoming less available for the LLMIC countries in Asia, Africa and Latin America. Furthermore, the global inequity of vaccine availability is compounded by certain high income countries starting to administer booster doses of the COVID vaccine despite majority of the population in the low-income countries having not yet even received a single dose [
      • Hannah Ritchie E.M.
      • Rodés-Guirao Lucas
      • Appel Cameron
      • Giattino Charlie
      • Ortiz-Ospina Esteban
      • Hasell Joe
      • Macdonald Bobbie
      • Beltekian Diana
      • Roser Max
      Coronavirus (COVID-19) vaccinations 2022.
      ].
      Presence of an infrastructure enabling efficient distribution and administration of the vaccines is a key requirement for the success of the COVID vaccination program. Most of the LLMICs do not have formal vaccination programs, lack data and records of individuals in need of vaccination, and do not have storage and distribution facilities to maintain ultra-cold chains required by some of the mRNA vaccines [
      • Peacocke EF
      • Heupink LF
      • Frønsdal K
      • Dahl EH
      • Chola L.
      Global access to COVID-19 vaccines: a scoping review of factors that may influence equitable access for low and middle-income countries.
      ,
      • Wouters OJ
      • Shadlen KC
      • Salcher-Konrad M
      • Aj Pollard
      • Larson HJ
      • Teerawattananon Y
      • et al.
      Challenges in ensuring global access to COVID-19 vaccines: production, affordability, allocation, and deployment.
      ].
      Furthermore, vaccine hesitancy has added to the challenges to the deployment of COVID-19 vaccines. Although vaccine hesitancy is prevalent in both high and low-income countries alike, certain factors such as mistrust in the allopathic medicines, suspicions of individuals from low-income countries being used as guinea pigs and low literacy rates may influence the vaccine hesitancy more in LLMIC countries. The resulting inefficient deployment of vaccines has led to vaccine wastage (eg, South Sudan and Malawi) or vaccine redeployment to avoid vaccine wastage (eg, the Democratic Republic of Congo to Ghana and Madagascar) in some of these countries [
      • Mwai P.
      2021 Covid-19 vaccines: Why some African states can't use their vaccines'.
      ].
      A survey was conducted recently by ISN and DOPPS to ascertain the availability, access and prioritization of COVID-19 vaccines globally [
      • Wijewickrama E
      • Bajpai D
      • Hafidz M
      • Robinson B
      • Johnson D
      • Liew A
      • et al.
      Availability and prioritization of covid-19 vaccines among patients with chronic kidney disease and kidney transplant-a global survey by the international society of nephrology.
      ]. This survey revealed that at least one COVID vaccine was available in almost all the countries surveyed. Patients with stage 4/5 CKD, dialysis and KTR were identified as priority group for COVID-19 vaccination and were vaccinated during the first two phases of the vaccination in 51%, 71% and 62% of the respondent countries. By August 2021 more than half of the countries surveyed had a vaccination rate of >50% for people with stage 4/5 CKD, dialysis and kidney transplants. However, there were significant variations according to the region and world bank income categories. For example, all respondents from Western Europe reported that over 50% of all kidney transplant recipients were vaccinated, whereas, in Africa and South East Asia, only a minority of respondents reported a >50% vaccination rate among kidney transplant recipients. The most common barriers to vaccination of kidney patients reported by respondents were vaccine hesitancy (74%), vaccine shortages (61%) and vaccine mass distribution challenges (48%) (Figure 4).
      Figure 4
      Figure 4Challenges encountered in COVID-19 vaccines to patients with kidney disease according income categories
      aThe percentage frequencies are based on responses by countries to: “How frequently are the following major challenges encountered in delivering COVID-19 vaccines to patients with kidney disease in your country?”
      bIf the response to the question on a particular challenge was either always, often or sometimes it was considered a major challenge
      *Total number of countries per income group is indicated in parentheses
      More equitable distribution of COVID-19 vaccines is the key to control the pandemic. According to a report by UN as of September 2021, just over 3% of people in LIC were vaccinated with at least one dose, compared to 60.18% in high income countries [
      • Yarlagadda H
      • Patel MA
      • Gupta V
      • Bansal T
      • Upadhyay S
      • Shaheen N
      • et al.
      COVID-19 Vaccine Challenges in Developing and Developed Countries.
      ]. By March 2022, of the more than 10 billion COVID-19 vaccines given out worldwide, only 1% has been administered in HIC highlighting the widening global inequality of COVID-19 vaccination.
      We need to do more work to overcome these growing inequalities in vaccination. Apart from strengthening the existing frameworks such as COVAX the high income countries need to share the know-how of the manufacturing of COVID-19 vaccines to low-income countries, in order to set up production facilities in these countries.
      One such initiative is the COVID-19 Technology Access Pool (C-TAP) launched by the WHO in May 2020 [
      • Tisi A.
      Patent rights or patient rights? An assessment of intellectual property and right to health within the Covid-19 pandemic.
      ]. It provides a single platform for the developers of COVID-19 vaccines, tests, devices and medicines to share their data, know-how and technologies with manufacturers. Policy makers should engage with communities to improve the public confidence and trust by combating the misinformation surrounding COVID-19 vaccination. Organizations such as UNICEF, that are already involved with well-conducted immunization programs in most of the low-income countries, could support the development of large scale COVID-19 vaccination programs in these countries.

      Conclusion

      Inequities in kidney care preceded the pandemic in LLMICs, however, the COVID-19 pandemic widened the gap even further and demonstrated a clear need for a global approach to care. Though LLMICs are improving in the diagnosis and management of COVID-19, barriers still remain. Efforts should be placed on improving the capacity of LLMICs to increase kidney care in general and vaccine equity to prevent transmission and decease the burden of COVID-19 infection.
      Advocacy to improve the care and management of kidney disease in LLMICs is needed for COVID-19 and beyond. The sequel of COVID-19 is still not clear and could lead to an increased prevalence of CKD. Further studies to assess the progress made so far in low income settings will also improve the care and management of COVID-19 associated kidney disease. Preparedness for future pandemics is also critical given the mortality and morbidity burden among patients with CKD.

      Financial support for this work

      The authors did not receive any external financial support for this work.

      Conflict of Interest

      The authors declare no conflict of interest

      Appendix. APPENDIX A. SUPPLEMENTARY MATERIAL

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