Factors Influencing Longevity of Humoral Response to SARS-CoV-2 Vaccination in Patients with End Stage Kidney Disease Receiving Renal Replacement Therapy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Vaccination Protocol
2.3. Anti-S-IgG Antibody Determination
2.4. Definitions
2.5. Ethical Issues
2.6. Statistical Analysis
3. Results
3.1. Study Population
3.2. Anti-SARS-CoV-2 Humoral Response following Vaccination
3.3. Predictive Factors of Anti-SARS-CoV-2 Humoral Response
3.4. Predictive Factors of Anti-S IgG Waning
4. Discussion
Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hilbrands, L.B.; Duivenvoorden, R.; Vart, P.; Franssen, C.F.M.; Hemmelder, M.H.; Jager, K.J.; Kieneker, L.M.; Noordzij, M.; Pena, M.J.; de Vries, H.; et al. COVID-19-Related Mortality in Kidney Transplant and Dialysis Patients: Results of the ERACODA Collaboration. Nephrol. Dial. Transpl. 2020, 35, 1973–1983. [Google Scholar] [CrossRef]
- Ng, J.H.; Hirsch, J.S.; Wanchoo, R.; Sachdeva, M.; Sakhiya, V.; Hong, S.; Jhaveri, K.D.; Fishbane, S. Northwell COVID-19 Research Consortium and the Northwell Nephrology COVID-19 Research Consortium Outcomes of Patients with End-Stage Kidney Disease Hospitalized with COVID-19. Kidney Int. 2020, 98, 1530–1539. [Google Scholar] [CrossRef]
- De Meester, J.; De Bacquer, D.; Naesens, M.; Meijers, B.; Couttenye, M.M.; De Vriese, A.S. NBVN Kidney Registry Group Incidence, Characteristics, and Outcome of COVID-19 in Adults on Kidney Replacement Therapy: A Regionwide Registry Study. J. Am. Soc. Nephrol. 2021, 32, 385–396. [Google Scholar] [CrossRef]
- Jahn, M.; Korth, J.; Dorsch, O.; Anastasiou, O.E.; Sorge-Hädicke, B.; Tyczynski, B.; Gäckler, A.; Witzke, O.; Dittmer, U.; Dolff, S.; et al. Humoral Response to SARS-CoV-2-Vaccination with BNT162b2 (Pfizer-BioNTech) in Patients on Hemodialysis. Vaccines 2021, 9, 360. [Google Scholar] [CrossRef]
- Clarke, C.L.; Prendecki, M.; Dhutia, A.; Gan, J.; Edwards, C.; Prout, V.; Lightstone, L.; Parker, E.; Marchesin, F.; Griffith, M.; et al. Longevity of SARS-CoV-2 Immune Responses in Hemodialysis Patients and Protection against Reinfection. Kidney Int. 2021, 99, 1470–1477. [Google Scholar] [CrossRef]
- Xie, Y.; Xu, E.; Bowe, B.; Al-Aly, Z. Long-Term Cardiovascular Outcomes of COVID-19. Nat. Med. 2022, 28, 583–590. [Google Scholar] [CrossRef]
- Torres-Castro, R.; Vasconcello-Castillo, L.; Alsina-Restoy, X.; Solis-Navarro, L.; Burgos, F.; Puppo, H.; Vilaró, J. Respiratory Function in Patients Post-Infection by COVID-19: A Systematic Review and Meta-Analysis. Pulmonology 2021, 27, 328–337. [Google Scholar] [CrossRef]
- Xie, Y.; Al-Aly, Z. Risks and Burdens of Incident Diabetes in Long COVID: A Cohort Study. Lancet Diabetes Endocrinol. 2022, 10, 311–321. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2020. [Google Scholar]
- Tylicki, L.; Biedunkiewicz, B.; Dąbrowska, M.; Ślizień, W.; Tylicki, P.; Polewska, K.; Rosenberg, I.; Rodak, S.; Dębska-Ślizień, A. Humoral Response to SARS-CoV-2 Vaccination Promises to Improve the Catastrophic Prognosis of Hemodialysis Patients as a Result of COVID-19: The COViNEPH Project. Pol. Arch. Intern. Med. 2021, 131, 797–801. [Google Scholar] [CrossRef]
- Rincon-Arevalo, H.; Choi, M.; Stefanski, A.-L.; Halleck, F.; Weber, U.; Szelinski, F.; Jahrsdörfer, B.; Schrezenmeier, H.; Ludwig, C.; Sattler, A.; et al. Impaired Humoral Immunity to SARS-CoV-2 BNT162b2 Vaccine in Kidney Transplant Recipients and Dialysis Patients. Sci. Immunol. 2021, 6, eabj1031. [Google Scholar] [CrossRef]
- Grupper, A.; Sharon, N.; Finn, T.; Cohen, R.; Israel, M.; Agbaria, A.; Rechavi, Y.; Schwartz, I.F.; Schwartz, D.; Lellouch, Y.; et al. Humoral Response to the Pfizer BNT162b2 Vaccine in Patients Undergoing Maintenance Hemodialysis. CJASN 2021, 16, 1037–1042. [Google Scholar] [CrossRef]
- Tauzin, A.; Gong, S.Y.; Beaudoin-Bussières, G.; Vézina, D.; Gasser, R.; Nault, L.; Marchitto, L.; Benlarbi, M.; Chatterjee, D.; Nayrac, M.; et al. Strong Humoral Immune Responses against SARS-CoV-2 Spike after BNT162b2 MRNA Vaccination with a 16-Week Interval between Doses. Cell Host Microbe 2022, 30, 97–109.e5. [Google Scholar] [CrossRef]
- Andreano, E.; Paciello, I.; Piccini, G.; Manganaro, N.; Pileri, P.; Hyseni, I.; Leonardi, M.; Pantano, E.; Abbiento, V.; Benincasa, L.; et al. Hybrid Immunity Improves B Cells and Antibodies against SARS-CoV-2 Variants. Nature 2021, 600, 530–535. [Google Scholar] [CrossRef]
- Biedunkiewicz, B.; Tylicki, L.; Ślizień, W.; Lichodziejewska-Niemierko, M.; Dąbrowska, M.; Kubanek, A.; Rodak, S.; Polewska, K.; Tylicki, P.; Renke, M.; et al. Waning Humoral Response after COVID-19 MRNA Vaccination in Maintenance Dialysis Patients and Recovery after a Complementary Third Dose. Vaccines 2022, 10, 433. [Google Scholar] [CrossRef]
- Levin, E.G.; Lustig, Y.; Cohen, C.; Fluss, R.; Indenbaum, V.; Amit, S.; Doolman, R.; Asraf, K.; Mendelson, E.; Ziv, A.; et al. Waning Immune Humoral Response to BNT162b2 COVID-19 Vaccine over 6 Months. N. Engl. J. Med. 2021, 385, e84. [Google Scholar] [CrossRef]
- Cho, A.; Muecksch, F.; Schaefer-Babajew, D.; Wang, Z.; Finkin, S.; Gaebler, C.; Ramos, V.; Cipolla, M.; Mendoza, P.; Agudelo, M.; et al. Anti-SARS-CoV-2 Receptor-Binding Domain Antibody Evolution after MRNA Vaccination. Nature 2021, 600, 517–522. [Google Scholar] [CrossRef]
- Davidovic, T.; Schimpf, J.; Abbassi-Nik, A.; Stockinger, R.; Sprenger-Mähr, H.; Lhotta, K.; Zitt, E. Waning Humoral Response 6 Months after SARS-CoV-2 Vaccination with the MRNA-BNT162b2 Vaccine in Hemodialysis Patients: Time for a Boost. Kidney Int. 2021, 100, 1334–1335. [Google Scholar] [CrossRef]
- Butsch, W.S.; Hajduk, A.; Cardel, M.I.; Donahoo, W.T.; Kyle, T.K.; Stanford, F.C.; Zeltser, L.M.; Kotz, C.M.; Jastreboff, A.M. COVID-19 Vaccines Are Effective in People with Obesity: A Position Statement from The Obesity Society. Obesity 2021, 29, 1575–1579. [Google Scholar] [CrossRef]
- Painter, S.D.; Ovsyannikova, I.G.; Poland, G.A. The Weight of Obesity on the Human Immune Response to Vaccination. Vaccine 2015, 33, 4422–4429. [Google Scholar] [CrossRef]
- Goldberg, Y.; Mandel, M.; Bar-On, Y.M.; Bodenheimer, O.; Freedman, L.S.; Ash, N.; Alroy-Preis, S.; Huppert, A.; Milo, R. Protection and Waning of Natural and Hybrid Immunity to SARS-CoV-2. N. Engl. J. Med. 2022, 386, 2201–2212. [Google Scholar] [CrossRef]
- Wang, Z.; Muecksch, F.; Schaefer-Babajew, D.; Finkin, S.; Viant, C.; Gaebler, C.; Hoffmann, H.-H.; Barnes, C.O.; Cipolla, M.; Ramos, V.; et al. Naturally Enhanced Neutralizing Breadth against SARS-CoV-2 One Year after Infection. Nature 2021, 595, 426–431. [Google Scholar] [CrossRef]
- Ioannou, G.N.; Locke, E.R.; Green, P.K.; Berry, K. Comparison of Moderna versus Pfizer-BioNTech COVID-19 Vaccine Outcomes: A Target Trial Emulation Study in the U.S. Veterans Affairs Healthcare System. eClinicalMedicine 2022, 45, 101326. [Google Scholar] [CrossRef]
A Time Point | |||
---|---|---|---|
Baseline (n = 191) | After 6 Months (n = 139) | After a Booster (n = 91) | |
Parameter | |||
Demographics | |||
Age (yrs. [Q1–Q3]) | 64.0 [53.0–70.5] | 65 [55.0–71.0] | 64.0 [56.0–72.0] |
Sex (females) n (%) | 122 (63.9) | 83 (59.7) | 57 (62.6%) |
Dialysis vintage (yrs [Q1–Q3]) | 2.99 [1.23–4.75] | 2.95 [1.25–4.76] | 2.82 [1.47–4.85] |
Comorbidities n (%) | |||
Obesity | 50 (26.2) | 40 (28.8) | 27 (29.7%) |
Diabetes mellitus | 59 (30.9) | 45 (32.4) | 25 (27.5%) |
Heart failure | 58 (30.4) | 47 (33.8) | 18 (19.8%) |
Hypertension | 176 (92.1) | 127 (91.4) | 81 (89.0%) |
Atrial fibrillation | 27 (14.1) | 24 (17.3) | 12 (13.2%) |
Prior COVID-19 | 72 (37.7) | 52 (37.4) | 32 (35.2%) |
Dialysis modality n (%) | |||
Peritoneal dialysis | 10 (5.2) | 1 (0.7) | 1 (1.1 %) |
Hemodialysis | 181 (94.8) | 138 (99.3) | 90 (98.9%) |
Type of Vaccine n (%) | |||
BNT162b2 | 109 (57.1) | 71 (51.1) | 44 (48.5%) |
mRNA-1273 | 82(42.9) | 68 (48.9) | 47 (51.6%) |
Laboratory, median [Q1–Q3] | |||
Hemoglobin (g/dL) | 10.7 [9.90–11.5] | 10.8 [9.90–11.6] | 10.9 [10.2–11.5] |
Kt/V | 1.40 [1.22–1.60] | 1.41 [1.23–1.61] | 1.40 [1.23–1.56] |
Variable of Interest | Independent Variable | β | SE | p |
Adequatehumoral response after the first dose | Age | 0.01 | 0.01 | 0.41 |
Sex (M) | 0.30 | 0.32 | 0.35 | |
Obesity | −0.34 | 0.35 | 0.34 | |
Diabetes mellitus | −0.35 | 0.33 | 0.30 | |
Hypertension | 0.95 | 0.66 | 0.15 | |
Heart failure | 0.33 | 0.32 | 0.31 | |
Atrial fibrillation | 0.33 | 0.42 | 0.44 | |
Kt/V | −0.97 | 0.48 | 0.04 | |
Hemoglobin | −0.13 | 0.12 | 0.29 | |
Dialysis modality (PD) | −0.36 | 0.71 | 0.61 | |
Vaccine type (BNT162b2) | 1.14 | 0.32 | 0.001 | |
Adequatehumoral response after the second dose | Independent Variable | β | SE | p |
Age | −0.01 | 0.03 | 0.80 | |
Sex (M) | 0.59 | 0.83 | 0.49 | |
Obesity | 0.59 | 1.11 | 0.60 | |
Diabetes mellitus | −0.12 | 0.88 | 0.90 | |
Hypertension | 0.89 | 1.13 | 0.43 | |
Heart failure | −0.86 | 0.83 | 0.30 | |
Atrial fibrillation | −0.20 | 1.12 | 0.86 | |
Kt/V | −0.88 | 1.26 | 0.49 | |
Hemoglobin | 0.03 | 0.33 | 0.93 | |
Dialysis modality (PD) | 15.19 | 2062.64 | 1.00 | |
Vaccine type (BNT162b2) | −0.42 | 0.88 | 0.63 | |
Adequatehumoral response after the third dose | Independent Variable | β | SE | p |
Age | 0.09 | 0.06 | 0.16 | |
Sex (M) | −17.25 | 3040.73 | 1.00 | |
Obesity | 17.13 | 3412.21 | 1.00 | |
Diabetes mellitus | 17.10 | 3546.07 | 1.00 | |
Hypertension | −15.89 | 3400.72 | 1.00 | |
Heart failure | 17.00 | 4179.09 | 1.00 | |
Atrial fibrillation | 16.00 | 3104.42 | 1.00 | |
Kt/V | 1.20 | 2.42 | 0.62 | |
Hemoglobin | 0.94 | 0.56 | 0.09 | |
Dialysis modality (PD) | 13.78 | 3956.18 | 1.00 | |
Vaccine type (BNT162b2) | −0.07 | 1.43 | 0.96 |
Variable of Interest | Predictor | OR (95%CI) |
---|---|---|
Univariable analysis | ||
anti-S IgG waning | Demographics | |
Age | 1.00 (0.97–1.03) | |
Sex | 1.03 (0.51–2.06) | |
Dialysis vintage | 0.97 (0.87–1.08) | |
Comorbidities | ||
Being obese | 3.47 (1.51–8.78) * | |
Diabetes mellitus | 1.90 (0.90–4.18) * | |
Heart failure | 1.19 (0.58–2.49) | |
Hypertension | 1.65 (0.49–5.54) | |
Atrial fibrillation | 1.07 (0.44–2.74) | |
History of COVID-19 infection before vaccination | 0.28 (0.13–0.57) * | |
Laboratory | ||
Hemoglobin (g/dL) | 1.34 (1.01–1.80) * | |
Kt/V | 0.89 (0.29–2.63) | |
Type of vaccine used (BNT162b2 vs. mRNA-1273) | 0.45 (0.22–0.89) * | |
Multivariable analysis | ||
anti-S IgG waning | History of COVID-19 infection before vaccination | 0.08 (0.02–0.29) |
Being obese | 3.25 (1.26–9.41) | |
Vaccination of a patient with prior COVID-19 infection with BNT162b2 | 11.51 (2.14–70.50) | |
Vaccination with BNT162b2 | 0.28 (0.10–0.80) | |
Being diabetic | 2.02 (0.85–4.98) | |
Higher Hb concentration | 1.28 (0.93–1.77) |
Variable of Interest | Predictor | OR (95%CI) |
---|---|---|
anti-S IgG waning | History of COVID-19 infection before vaccination | 0.09 (0.02–0.33) |
Being obese | 3.87 (1.44–11.99) | |
Vaccination of a patient with prior COVID-19 infection with BNT162b2 | 9.53 (1.70–60.67) | |
Vaccination with BNT162b2 | 0.37 (0.12–1.09) | |
Being diabetic | 1.69 (0.70–4.22) | |
Higher Hb concentration | 1.34 (0.97–1.89) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Glowinska, I.; Labij-Reduta, B.; Juzwiuk, J.; Lukaszewicz, M.; Pietruczuk, A.; Poplawska, A.; Daniluk-Jamro, A.; Kakareko, K.; Rydzewska-Rosolowska, A.; Naumnik, B.; et al. Factors Influencing Longevity of Humoral Response to SARS-CoV-2 Vaccination in Patients with End Stage Kidney Disease Receiving Renal Replacement Therapy. J. Clin. Med. 2022, 11, 4984. https://doi.org/10.3390/jcm11174984
Glowinska I, Labij-Reduta B, Juzwiuk J, Lukaszewicz M, Pietruczuk A, Poplawska A, Daniluk-Jamro A, Kakareko K, Rydzewska-Rosolowska A, Naumnik B, et al. Factors Influencing Longevity of Humoral Response to SARS-CoV-2 Vaccination in Patients with End Stage Kidney Disease Receiving Renal Replacement Therapy. Journal of Clinical Medicine. 2022; 11(17):4984. https://doi.org/10.3390/jcm11174984
Chicago/Turabian StyleGlowinska, Irena, Barbara Labij-Reduta, Jerzy Juzwiuk, Magdalena Lukaszewicz, Adam Pietruczuk, Agata Poplawska, Anna Daniluk-Jamro, Katarzyna Kakareko, Alicja Rydzewska-Rosolowska, Beata Naumnik, and et al. 2022. "Factors Influencing Longevity of Humoral Response to SARS-CoV-2 Vaccination in Patients with End Stage Kidney Disease Receiving Renal Replacement Therapy" Journal of Clinical Medicine 11, no. 17: 4984. https://doi.org/10.3390/jcm11174984
APA StyleGlowinska, I., Labij-Reduta, B., Juzwiuk, J., Lukaszewicz, M., Pietruczuk, A., Poplawska, A., Daniluk-Jamro, A., Kakareko, K., Rydzewska-Rosolowska, A., Naumnik, B., Koc-Zorawska, E., Zorawski, M., & Hryszko, T. (2022). Factors Influencing Longevity of Humoral Response to SARS-CoV-2 Vaccination in Patients with End Stage Kidney Disease Receiving Renal Replacement Therapy. Journal of Clinical Medicine, 11(17), 4984. https://doi.org/10.3390/jcm11174984