https://orcid.org/0000-0001-6681-8479
Figures
Abstract
Background
The newly developed COVID-19 vaccines are highly effective and safe. However, a small portion of vaccine recipients experience a wide range of adverse events. Recently, glomerular disease, including the development of Minimal Change Disease (MCD), has been observed after administration of different COVID-19 vaccines, although causality remains a matter of debate.
Aim
The aim of this systematic review was to comprehensively examine the available literature and provide an overview of reported cases of MCD following vaccination against SARS-CoV-2.
Results
We identified 46 eligible articles which included 94 cases with MCD following COVID-19 vaccination of which one case was reported twice due to a second relapse. Fifty-five participants were males (59.1%, 55/93) and 38 (40.9%, 38/93) were females with a mean age of 45.02 years (SD:20.95). From the included patients 50 (50/94, 53.1%) were described as new-onset and 44 (46.9%, 44/94) as relapse. On average, symptomatology developed 16.68 days (SD: 22.85) after the administration of the vaccine irrespective of the dose. Data about symptoms was reported in 68 cases with the most common being oedema (80.8%, 55/68), followed by weight gain (26.5%, 18/68) and hypertension (16.1%, 11/68). In terms of outcome, more than half of the patients went into remission (61%, 57/94), while 18 recovered or improved post treatment (19.1%, 18/94). Two people relapsed after treatment (2.1%, 2/94) and two cases (2.1%, 2/94) were reported as not recovered.
Conclusion
MCD is possibly a condition clinicians may see in patients receiving COVID-19 vaccines. Although this adverse event is uncommon, considering the limited published data and the absence of confirmed causality, increased clinical awareness is crucial for the early recognition and optimal management of these patients.
Citation: Kechagias KS, Laleye JD, Drmota J, Geropoulos G, Kyrtsonis G, Zafeiri M, et al. (2024) Minimal change disease following COVID-19 vaccination: A systematic review. PLoS ONE 19(3): e0297568. https://doi.org/10.1371/journal.pone.0297568
Editor: Rajendra Bhimma, University of KwaZulu-Natal, SOUTH AFRICA
Received: May 12, 2023; Accepted: January 4, 2024; Published: March 5, 2024
Copyright: © 2024 Kechagias et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
In late 2019, a global pandemic, which created extraordinary socio-economic consequences, emerged due to an outbreak of an uncommon viral pneumonia [1–3]. The aetiological factor was later identified as a previously unknown strain of coronavirus named Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), responsible for the onset of coronavirus disease 2019 (COVID-19). The disease has since spread extensively, impacting hundreds of millions of individuals across the globe [4, 5].
Various vaccines have been utilised successfully against SARS-CoV-2 such as COMIRNATY (BioNTech-Pfizer’s COVID-19 mRNA vaccine BNT162b2), COVID-19 Vaccine Moderna (Moderna’s mRNA vaccine-1273), VAXZEVRIA (AstraZeneca-Oxford University’s ChAdOx1-nCoV19), COVID-19 Vaccine Janssen (Janssen’s Ad26.COV2.S) and CoronaVac COVID19 vaccine (Sinovac Biotech’s Vero cell) [6, 7]. Currently, nearly two-thirds of the global population have received at least one dose of a COVID-19 vaccine, with more than 13 billion doses administered worldwide [8].
A plethora of published studies have demonstrated the safety and effectiveness of the aforementioned vaccines, with only infrequent adverse events reported in the literature [9–12]. Nonetheless, isolated adverse reactions after COVID-19 vaccine administration are unavoidable, given the vast amount of vaccination doses needed to curb the spread of COVID-19 [13, 14]. At present, patients commonly experience various reported adverse symptoms, such as muscle pain, fever, headache, nausea, and vomiting. In addition to the frequently observed adverse effects following COVID-19 vaccination, patients have also reported a wide range of complaints and symptoms, including immune-mediated adverse events [13, 15–18].
Recently, there is a growing number of reports regarding the development of Minimal Change Disease (MCD) in patients following their initial or second COVID-19 vaccine doses; However, these cases have not yet undergone thorough investigation, and the administration of COVID-19 vaccines has not been recognised as a causative factor for renal dysfunction. To address this gap, our study systematically analysed the existing literature to present a comprehensive summary of documented cases of MCD following SARS-CoV-2 vaccination.
Methods
This review was reported based on the “Preferred Reporting Items for Systematic Reviews and Meta-Analyses” (PRISMA) guidelines (S1 Fig).
Literature search
Two reviewers (KSK, JDL) searched PubMed and Scopus library databases from inception until January 2023 independently. The search included the following terms: “(COVID 19 vaccin* OR SARS-COV2 vaccin*) AND (minimal change disease OR glomerulonephritis OR nephrotic OR nephritic)”. There were no limitations placed regarding study design, geographic region, or language. Additionally, a manual search of references cited in the included articles and relevant published reviews was conducted to identify any missed studies. Discrepancies during the literature search were resolved by a third investigator (DS).
Eligibility criteria
We included studies that provided data for new onset or relapse of MCD following COVID-19 vaccination with at least one dose. All study designs were considered eligible for inclusion. Review articles, abstracts submitted in conferences and non-peer reviewed sources were not eligible for inclusion. Studies on in vitro and animal models were excluded.
Data extraction and handling
In all studies, patient data was retrieved and handled by two authors (JDL, JD) who conducted the data extraction independently. We collected the following information: sex, age, comorbidities, vaccine type, number of doses received, presenting complains and symptoms, history of previous COVID-19 infection, laboratory tests including antibodies, primary diagnosis, imaging findings, therapeutic management and clinical outcome. Any disagreements were discussed and resolved by a third author (KSK).
Quality assessment
The quality of the included studies was assessed using the criteria established by the Task Force for Reporting Adverse Events of the International Society for Pharmacoepidemiology (ISPE) and the International Society of Pharmacovigilance (ISoP) [19]. The evaluation was based on the satisfactory reporting of 12 different elements, including the title, patient demographics, current health status, medical history, physical examination, patient disposition, drug identification, dosage, administration/drug reaction interface, concomitant therapies, adverse events, and discussion. Each element was assigned a score of either 0 (lack of information) or 1 (information present) for the studies.
Results
Study characteristics
The initial literature search yielded 830 publications. In the first screening 777 studies were excluded as irrelevant. Forty-six studies [20–65] were found to be eligible for the systematic review based on the predefined inclusion criteria (Fig 1). Twenty of the studies were conducted in Asia, 16 in Europe, 9 in Americas, and 1 in Australia. Seven studies were case series and 39 were case reports (Table 1).
IPD: individual patient data.
We identified a total of 94 cases of MCD following COVID-19 vaccination, of which one case was reported twice after relapsing following the second dose.
Fifty-five participants were males (59.1%, 55/93) and 38 (40.9%, 38/93) were females with a mean age of 45.02 years (SD:20.95). From the included patients 50 (50/94, 53.1%) were characterised as new-onset and 44 (46.9%, 44/94) as relapse. The mean age of individuals with MCD relapse was 41.6 (SD:20). For most of the patients (79.5%, 74/93) data regarding COVID-19 infection before or at the time of diagnosis was not provided. Among the remaining patients only 2 were previously infected with SARS-CoV-2. In 2 cases, vaccine brand was not reported (2.1%, 2/94). The majority of the patients received COMIRNATY (58.5%, 55/94), followed by COVID-19 Vaccine Moderna (20.2%, 19/94) and VAXZEVRIA (14%, 13/94), while 4 participants received COVID-19 Vaccine Janssen (3.2%, 3/94) and CoronaVac (1%, 1/94). In one case vaccine type was reported as modRNA (1%, 1/94). The majority of patients developed symptoms after the first dose (55.5%, 52/94), followed by the second dose (39.3%, 37/94), third dose (2.2%, 2/94), booster (1%, 1/94), both first and second doses (1%, 1/94), while in one case relevant data was not provided (1%, 1/94).
On average, the symptoms developed 16.68 days (SD: 22.85) after the administration of the vaccine irrespective of the dose. Data about symptomatology was reported in 68 individuals with the most common symptom being oedema (80.8%, 55/68), weight gain (26.5%, 18/68) and hypertension (16.1%, 11/68). MCD was confirmed with biopsy in 76 cases (80.8%, 76/94). Sixteen cases (17%, 16/94) were relapses and biopsy was not repeated. In two cases (2.1%), diagnosis was based on clinical suspicion (S1 Table). The majority of patients received steroids (91.5%, 86/94), while some patients were treated with immunosuppressive agents (22.3%, 21/94) and diuretics (17%, 16/94). More than half went to remission (61%, 57/94), while 18 achieved recovery or improved following treatment (19.1%, 18/94). Two people relapsed after treatment (2.1%, 2/94) and two cases (2.1%, 2/94) were reported as not recovered. In 15 cases (16%, 15/94) data about outcome was not provided.
Quality of the studies
The mean quality score indicated that the studies reported on average 10 of the recommended 12 elements, defined by the guidelines. Ten studies had a perfect score of 12 while the second most common score was 11 (S2 Table).
Discussion
The administration of COVID-19 vaccines has not been deemed as a causative factor for kidney disease. However, recent findings, primarily derived from case reports and case series, indicate that various kidney disorders such as Minimal Change Disease (MCD), IgA nephropathy, membranous glomerulopathy, and IgG4-related disease have been observed to initially manifest or relapse subsequent to SARS-CoV-2 vaccination. These observations suggest a potential link between COVID-19 vaccination and the occurrence or recurrence of MCD. In this study, we conducted a thorough screening of the existing literature to present a comprehensive summary of documented cases of MCD following SARS-CoV-2 vaccination. Our systematic review identified 46 relevant reports, involving a total of 93 patients, in which MCD was observed subsequent to the administration of various COVID-19 vaccines. In the majority of cases, symptoms began to emerge following the first vaccine dose, and clinical improvement was reported for most patients.
Results in the context of the literature
MCD consists the most frequent cause of nephrotic syndrome in childhood and rarely affects adults. MCD generally presents with a sudden onset of symptoms and signs of nephrotic syndrome and requires histologic confirmation in adults. Its pathogenesis remains to be elucidated, however, evidence points towards T cell dysfunction being a major mechanism [66]. It has been previously proposed that a glomerular permeability factor is produced, attacks the glomerular filtration barrier and leads to the destruction of podocytes and subsequent proteinuria. It’s most commonly idiopathic, but infections, medications, vaccinations, malignancies, and allergens are among the secondary etiologic factors [67]. Infections including syphilis, hepatitis C and tuberculosis, and vaccinations against hepatitis B, influenza, measles and rubella are established triggering factors for the relapse of primary glomerulonephritis, potentially with a similar mechanism involved in the development of MCD [68].
In animal models the prevalence of CD8+ suppressor T-cells and subsequent cytokine-induced injury has been observed in the active phase of MCD [60, 69]. This could provide a possible explanation for the aforementioned cases since the existent vaccinations against COVID-19 are known to strongly induce T-cell activation and this could lead to immune mediated podocyte damage. It’s worth noting that during the vaccine-induced T-cell activation, interferon gamma and inerleukin-2 (IL-2) are increased and IL-2 has been found to be raised in the acute phase and relapses of idiopathic nephrotic syndrome [22]. Direct podocyte injury could also be implicated in MCD in both COVID-19 infection and vaccination and interestingly ACE-2 is expressed in podocytes, however there is currently not adequate evidence to establish a causative mechanism. Moreover, similarities between vaccine adjuvants and human proteins could lead to immune cross-reactivity and drug-induced hypersensitivity reactions through molecular mimicry [70, 71].
Even though MCD most commonly presents during childhood, it has been reported mainly in adults following COVID-19 vaccination, however this is to be expected considering the high vaccination rates in these age groups. MCD symptomatology commenced within 3 weeks from the first dose in more than half of the patients, although a significant amount of people developed symptoms after the second dose, which could be associated to the amplitude of the immune response. Symptoms did not differ from those commonly reported in literature and glucocorticoids were chosen as first-line treatment in 91.5% of the cases. Concerns about potential interference of immunosuppressive agents such as rituximab in the vaccination efficacy has been raised, however, relevant treatment to achieve best clinical response should be prioritised over immunisation in these cases. Overall the vast majority responded to treatment and maintained positive outcomes.
Strengths and limitations
Our study represents the first systematic review conducted on the relationship between COVID-19 vaccination and the occurrence or relapse of MCD. Our findings present a comprehensive overview of published reports with quality assessment of the included studies.
However, it is important to highlight certain limitations linked to our study. One major limitation stems from the low quality nature of the case reports and case series included in this review, which can impact the validity and generalizability of the conclusions. These studies are susceptible to potential biases including overinterpretation and selection bias. Consequently, while the reported findings are interesting, they may not necessarily provide an accurate representation of the true effect of COVID-19 vaccination in relation to renal dysfunction. Therefore, establishing causality requires insight from mechanistic studies and well-designed appropriately powered prospective studies.
Conclusion
While the current COVID-19 vaccines are generally considered safe and the advantages of vaccination outweigh the potential occurrence of adverse events, it is possible for patients to develop mild to moderate side effects, including complications related to renal dysfunction. Minimal change disease is possibly a condition clinical doctors and other healthcare professionals may expect to see in patients receiving COVID-19 vaccines. Although this adverse event is uncommon, considering the limited published data and the absence of confirmed causality, increased clinical awareness is crucial for the early recognition and optimal management of these patients.
Supporting information
S1 Table. Laboratory results and imaging findings for the included cases.
https://doi.org/10.1371/journal.pone.0297568.s001
(DOCX)
S2 Table. Quality assessment of the included studies.
https://doi.org/10.1371/journal.pone.0297568.s002
(DOCX)
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