As of November 2021, the coronavirus disease 2019 (COVID-19) pandemic has claimed >5 million lives worldwide, with >750,000 deaths in the United States (1). The three vaccines currently authorized for use by the Food and Drug Administration, either with approval or emergency use authorization, are all highly effective at preventing death and serious illness in the general population (2–4).
Concerns about the robustness of the vaccine-induced immune response in vulnerable populations (H. Chemaitelly et al., unpublished data) (5,6) have prompted the Centers for Disease Control and Prevention (CDC) to recommend an additional dose for patients who are immunocompromised (7), and concerns about the durability of response have prompted guidance on booster doses of vaccine (8). Early studies suggest that the majority of patients receiving maintenance dialysis generate an appropriate initial seroresponse to mRNA vaccines, although at a lower rate than the general population (9–16). Given that patients on maintenance dialysis have an attenuated response to other vaccines, with extensive data on additional or booster doses for hepatitis B vaccination (17), similar concerns exist that potential uremia-associated immunocompromise may affect the response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines. A small study in 76 patients on dialysis demonstrated anti-spike IgG antibody decline in 75% of patients, with almost 20% becoming seronegative by 4 months (A. Dulovic et al., unpublished data). In the general population, waning immunity has been linked to increased breakthrough cases (18,19). Given the very high risk for poor outcomes associated with COVID-19 in patients on maintenance dialysis, and their limited ability to physically distance, obtaining and maintaining immunity is of critical importance (20,21). Therefore, we conducted a retrospective, multicenter study to assess the intermediate duration of vaccine-induced seroresponse among patients receiving maintenance dialysis. Expanding on an earlier publication (10), we report here the seroresponse trends over time.
Materials and Methods
Dialysis Clinic, Inc. (DCI) is a national not-for-profit provider that cares for >15,000 patients at 260 outpatient dialysis clinics across 29 states. Since January 2021, physicians at DCI facilities have had available an antibody-monitoring protocol for patients, activated by physician order upon documentation of receipt of a SARS-CoV-2 vaccine, regardless of the vaccine type or place of administration. Like the existing hepatitis B vaccine protocol, the SARS-CoV-2 vaccine protocol documents seroresponse to vaccination by measuring antibody titers as part of the monthly blood draws. IgG spike antibodies (anti-spike IgG) against the receptor-binding domain of the S1 subunit of the SARS-CoV-2 spike antigen were measured using the chemiluminescent assay ADVIA Centaur XP/XPT COV2G, which received emergency use authorization in July 2020 (22). This semiquantitative assay reports an Index Value between zero and ≥20 established with calibrators; per manufacturer specifications, anti-spike IgG titer ≥1 Index represents detectable antibodies, likely signifying seroresponse (22).
Demographic and clinical data, vaccination dates, and anti-spike IgG titer results were obtained from the DCI electronic health record. Patients were included if they had received a complete vaccine series of one vaccine type without additional doses. Patients were excluded from analysis if they were <18 years of age or did not have at least one antibody titer assessment ≥14 days after completion of a vaccine series (hereafter termed “fully vaccinated” in accordance with current CDC guidelines ). Baseline characteristics were assessed at the time of full vaccination. Prior COVID-19 was defined by a positive SARS-CoV-2 PCR test at any time before the date of full vaccination or anti-spike IgG titer ≥1 Index before or within 10 days after the first vaccine dose (representing likely prior undiagnosed COVID-19, as suggested by prior studies [2,24]). Through a DCI protocol, which has been active since March 2020, positive SARS-CoV-2 tests were captured regardless of whether the patient was assessed in the dialysis clinic, at a testing center, or at a hospital. Antibody test results were captured from only the DCI dialysis clinics. Analyses were stratified by prior COVID-19 status.
In analyses, anti-spike IgG titers were grouped by the month of assessment relative to the date of full vaccination (month 1, 2, etc.). Primary descriptive analyses compared titers by vaccine type over time. To assess whether initial vaccine response was associated with sustained response, secondary descriptive analyses compared trends over time, stratifying by the maximum titer attained during the first 2 months after full vaccination (“maximum initial titer”). Handling of missing and duplicate values is described in Supplemental Appendix 1.
To better characterize antibody levels over time, time-to-event analysis was used to assess for the outcome of antibody titer <1 Index or development of COVID-19, defined as having a positive SARS-CoV-2 test. Two sets of sensitivity analyses were conducted. The first used the outcome of antibody titer <2 Index or development of COVID-19, using a threshold suggested by the DCI laboratory’s internal validation methods (10). The second used the outcome of antibody titer <1 Index alone. Of note, all patients dialyzing in DCI facilities are screened for COVID-19 symptoms and recent exposure upon arrival to the dialysis facility for each treatment, followed by SARS-CoV-2 testing if they screen positive. Patients were censored at death, transplantation, administration of an additional vaccine dose (third dose or booster dose), or last available titer assessment. Results were compared by vaccine type and by maximum initial titer in descriptive analyses. The association of patients’ clinical characteristics with time to the outcome was assessed using multivariable Cox proportional hazards regression; covariates were selected a priori on the basis of clinical relevance and availability in the dataset.
This study was reviewed and approved by the WCG Institutional Review Board Work Order 1-1456342-1. Statistical analyses were performed using R version 4.0.2.
Among patients receiving maintenance dialysis at a DCI facility, 1898 adults across 142 clinics received a full SARS-CoV-2 vaccine series and had at least one anti-spike IgG titer assessment after January 1, 2021, with 1870 patients having anti-spike IgG assessment after full vaccination (Figure 1). Of these, 1087 (58%) were men, 438 (23%) were Black, 301 (16%) were Hispanic, and the average±SD age was 64±14 years; 301 (16%) patients had a history of COVID-19 on the basis of either early positive anti-spike IgG levels or prior clinical diagnosis. Antibody assessment tended to be clustered by clinic, with 80% of patients being treated in 30 DCI clinics. Recipients of BNT162b2 (Pfizer) tended to be older and have longer follow-up, whereas recipients of Ad26.COV2.S (Janssen) were more often of Black race. Among the 1569 patients without a history of COVID-19, a higher proportion of recipients of mRNA-1273 (Moderna) were receiving peritoneal dialysis compared with recipients of BNT162b2 and Ad26.COV2.S (Table 1).
Table 1. -
Baseline patient characteristics by history of coronavirus disease 2019 and type of vaccine received
||All Vaccinated DCI Patients (N=11,668)
||No History of COVID-19 (N=1569)
||History of COVID-19 (N=301)
| Native American
| Asian/Pacific Islander
|Body mass index, kg/m2
|Long-term care facility
| Home hemodialysis
| In-center hemodialysis
| Peritoneal dialysis
|HBsAb ≥10 mIU/ml
|History of transplantation
|Congestive heart failure
|Peripheral vascular disease
|Chronic obstructive pulmonary disease
|History of cancer
|Duration of follow-up, d
Vintage and duration of follow-up are reported as median (interquartile range). All other data are reported as mean±SD or n (%). Data on baseline patient characteristics were complete. COVID-19, coronavirus disease 2019; DCI, Dialysis Clinic, Inc.; HBsAb, hepatitis B surface antibody.
aPatients fully vaccinated with an emergency use–approved vaccine series of one type without additional doses before August 13, 2021.
bInadequate dialysis defined by hemodialysis dose single-pool Kt/V <1.2 or peritoneal dialysis dose weekly Kt/V <1.7.
cHBsAb ≥10 mIU/ml signifies hepatitis B seroimmunity.
dImmunomodulating medications include anti-inflammatory medications, antineoplastic agents, corticosteroids, and certain anti-infective medications.
Patients without a history of COVID-19 who received an mRNA vaccine had declining anti-spike IgG titers over time (Figure 2A). Among recipients of BNT162b2, the median (interquartile range [IQR]; number of data values [N]) antibody titer was ≥20 (5.89 to ≥20; N=340) Index in month 1 after full vaccination, with a reduction to 3.16 (0.82–10.59; N=379) by month 4 and 1.96 (0.60–5.88; N=244) Index by month 6. Among recipients of mRNA-1273, median (IQR; N) anti-spike IgG titer declined from ≥20 (≥20 to ≥20; N=645) in month 1 to ≥20 (4.14 to ≥20; N=649) by month 4 and to 7.99 (2.61 to ≥20; N=439) by month 6. Over all time periods, recipients of Ad26.COV2.S had median anti-spike IgG titers of <1 Index, without a significant change over time. Among patients with a history of COVID-19, >75% maintained antibody titer at the upper limit of the assay’s detection (≥20 Index) through month 6 (Figure 2B).
Among the 1569 patients without a history of COVID-19, 613 developed anti-spike IgG titer <1 Index or were diagnosed with COVID-19 (589 and 24 patients, respectively). Time-to-event analysis showed a difference by vaccine type, with recipients of Ad26COV2.S having the shortest time to anti-spike IgG <1 Index, whereas recipients of mRNA-1273 had more durable anti-spike IgG titer levels (Figure 3). At month 4, 67% of Ad26.COV2.S, 29% of BNT162b2, and 11% of mRNA-1273 recipients had anti-spike IgG titers <1 Index; at month 6, 52% of Ad26.COV2.S, 33% of BNT162b2, and 10% of mRNA-1273 recipients had anti-spike IgG titers of <1 Index. Sensitivity analysis using the threshold of anti-spike IgG titer <2 Index instead showed more events occurring, as expected, but the differences by vaccine type remained (Supplemental Figure 1). Results changed minimally in sensitivity analysis using the outcome of anti-spike IgG titer <1 Index alone (Supplemental Figure 2).
To assess whether initial seroresponse is associated with sustained response, patients were then grouped by maximum titer measured during the first 2 months after full vaccination: 866, 345, and 302 patients had maximum initial titer of ≥20, 1 to <20, and <1 Index, respectively, whereas 56 patients did not have a titer assessed during the first 2 months of full immunity and were excluded from this analysis. Baseline characteristics by maximum initial titer are shown in Supplemental Table 1. In time-to-event analysis, those who had a maximum initial titer ≥20 Index were less likely to develop the outcome of titer <1 Index or COVID-19 compared with those with a maximum initial titer from 1 to 19.99 Index. This difference persisted even among recipients of the same vaccine type (Figure 4), in sensitivity analyses for the outcome of titer <2 Index (with corresponding change in strata thresholds; Supplemental Figure 3), and in sensitivity analyses for the outcome of titer <1 Index alone (Supplemental Figure 4). In multivariable Cox proportional hazards regression, in addition to differences by vaccine type, older age, White race, higher body mass index, lower albumin, lack of hepatitis B seroimmunity, and use of immunomodulating medications were associated with shorter time to loss of seroresponse (Figure 5). In sensitivity analysis using the outcome of titer <2 Index, body mass index was no longer associated with loss of seroresponse; other findings were similar (Supplemental Figure 5). Results were minimally changed in sensitivity analysis using the outcome of titer <1 Index alone (Supplemental Figure 6).
Among a national population of patients receiving maintenance dialysis, mRNA vaccines elicited greater seroresponse than the Ad26.COV2.S vaccine, but antibody titers against the SARS-CoV-2 spike protein waned substantially over the first 6 months after full vaccination among patients without a prior history of COVID-19. Furthermore, the robustness of the initial antibody response is associated with the rapidity of subsequent waning of antibody levels. Other clinical factors associated with the duration of seroresponse largely reflect patients’ immune health.
As of December 2021, the CDC has issued recommendations for booster doses of SARS-CoV-2 vaccine, prompted by concerns about the durability of vaccine response (8). In particular, patients receiving maintenance dialysis have had an attenuated response to other vaccines (17) and are at high risk for poor outcomes during the COVID-19 pandemic (21). Critically, initial studies suggest that vaccine-induced immunity among patients on maintenance dialysis immediately after receipt of a vaccine series was intermediate, with somewhat lesser response than among the general population, but a greater response than among patients receiving immunosuppression for transplantation or other indications (9–16). Our data provide longitudinal evidence of immunity waning fairly rapidly over time, with about half of patients on maintenance dialysis developing undetectable antibody protection at 6 months after full vaccination. Data from both the initial vaccine trials and more recent real-world observational studies show some waning of anti-spike IgG titers over time in healthy adults, although the magnitude of the decline has varied greatly between studies (25–31). Although the antibody level needed for protection from disease has not been definitively determined, a general correlation between seroimmunity and protection from disease has been observed (32). Additionally, individuals with seroimmunity may be less likely to transmit the virus, providing protection to other vulnerable patients in mandatory congregate health care settings (O. Prunas et al., unpublished data) (33). Similar data on waning immunity prompted officials in France to recommend an additional vaccine dose to patients on maintenance dialysis in April 2021, with some early evidence of subsequent strengthened immunity in several small studies (24,34–36).
There may be a role for wider routine monitoring of anti-spike IgG titers for patients on maintenance dialysis. Seroimmunity to hepatitis B is currently monitored through such a protocol, and, due to this population’s regular and frequent contact with the medical system, routine testing and administration of additional doses would not be logistically difficult. In particular, the peak response in the first 2 months of full immunity indicates the patient’s likely course and could be used to anticipate the timing of loss of seroimmunity (28). Of note, the CDC currently does not recommend using COVID-19 antibody testing to guide clinical decision making (37).
The apparent association of Black race with greater durability of seroresponse in this study may partially reflect the multivariable model’s simultaneous adjustment for vaccine type, given that a disproportionately large fraction of recipients of Ad26.COV2.S were of Black race. However, this association persisted when the analyses were restricted to only recipients of an mRNA vaccine. This association has been also observed in our prior work (38) and requires further investigation.
This study represents a real-world, geographically diverse, multicenter population of patients receiving maintenance dialysis in the United States, in whom prior risk of COVID-19 morbidity and mortality has been documented (21,39). We acknowledge this study’s limitations. The antibody-monitoring protocol was more widely used by clinics with earlier vaccine administration, reflecting the early uncertainty around the vaccine’s effectiveness among patients on maintenance dialysis. This clinic-clustering use of the protocol may have induced a selection bias, although it is ameliorated by the bias occurring at the level of the clinics rather than the individual patient. As with all observational studies, confounding variables may affect interpretation of results. In particular, data for months 5 and 6 primarily reflect patients who received their vaccine doses early (e.g., January through March of 2021), with a moderately higher proportion of recipients of mRNA vaccines, and these patients may be frailer at baseline. Patients without a baseline titer assessment may have been misclassified with respect to their COVID-19 history. We further acknowledge that missing data may have biased results. In addition, we did not correlate antibody titers with breakthrough infection, an issue that remains complex and controversial.
In conclusion, immunity to SARS-CoV-2 vaccines, as indicated by anti-spike IgG titers, wanes over time among patients on maintenance dialysis who do not have a prior history of COVID-19. In the setting of SARS-CoV-2 variants of concern, the effect of waning titers on breakthrough infections needs to be monitored closely. The current CDC recommendation to provide a third vaccine dose on the basis of clinical assessment for immunocompromise is an important consideration for the maintenance dialysis population. A large proportion of patients receiving maintenance dialysis have suboptimal response to the currently recommended vaccine regimens. Therefore, additional doses of vaccine should be considered for this vulnerable population, whether routinely or, with further investigation, potentially guided by protective correlates, such as antibody response.
K. Abreo reports serving as a scientific advisor or member of the editorial boards of Clinical Nephrology, Journal of Vascular Access, and Open Journal of Urology and Nephrology; receiving salary support to his institution from DCI; and serving as a member of the Vascular Access Task Force of Nephrologist Transforming Dialysis Safety. C. Argyropoulos reports having other interests/relationships with AbbVie (as subinvestigator in a phase 3 study of an experimental agent in diabetic nephropathy), with Akebia (as the principal investigator [PI] in two phase 3 trials of an investigational product for the correction and maintenance of anemia in patients with nondialysis-dependent CKD and one phase 3 study of the same agent in dialysis), with DCI (as the medical director of the outpatient dialysis unit in Cuba, New Mexico), and with Dialysis Outcomes and Practice Patterns Study (DOPPS; as PI for CKD-DOPPS); having consultancy agreements with Alkahest and Momenta Pharma; serving as a scientific advisor or member of Baxter Healthcare, Bayer, and Health Services Advisory Group; receiving salary support to his institution from DCI; and receiving research funding from DCI and University of Pennsylvania. G.N. Aweh, J. Frament, E.K. Lacson, and H.J. Manley report being employees of DCI. A. Chin reports receiving salary support to his institution from DCI, having other interests/relationships as medical director of a dialysis clinic owned by DCI, and serving as a scientific advisor or member of the National Quality Forum Renal Committee. R. Gladish reports receiving salary support to his institution from DCI and being employed by Nephrology of North Alabama. D. Johnson reports being employed by DCI, serving as vice chair of the board at DCI, and serving in an advisory or leadership role with Alive Hospice and the American Association of Kidney Patients. V. Ladik reports having ownership interest in American Airlines and Sunrun Inc., and being employed by DCI. D. Miskulin reports serving as an associate editor of CJASN; being employed by DCI; and receiving research funding from DCI, Reata Inc., and Regulus Inc. L. Salman reports receiving research funding from Albany Medical Center, Roach, and Transonics Inc.; having other interests/relationships with the American Society of Diagnostic and Interventional Nephrology, American Society of Nephrology (ASN), the data safety monitoring board of Phraxis, and the Renal Physician Association; receiving salary support to his institution from DCI; and having a patent application for the use of 4-methylumbelliferone in diabetic kidney disease. D.E. Weiner reports receiving honoraria from Akebia paid to DCI for participation in medical advisory boards; participating in medical advisory boards for Cara Therapeutics (2020), Janssen Biopharmaceuticals (2019), and Tricida (2019); serving as a member of the ASN Quality and Policy Committees, ASN representative to Kidney Care Partners, Medical Director of Clinical Research at DCI, editor-in-chief of Kidney Medicine, and coeditor-in-chief of National Kidney Foundation (NKF)’s Primer on Kidney Diseases (8th edition); serving as a member of the data monitoring committee of the “Feasibility of Hemodialysis with GARNET in Chronic Hemodialysis Patients with a Bloodstream Infection” Trial (Avania clinical research organization [CRO]), on the scientific advisory board of the NKF, and as the chair of adjudications committee of the VALOR Trial (George Institute, CRO); receiving salary support to his institution from DCI; receiving research funding from DCI as site PI for trials contracted with DCI, including Ardelyx (completed) and Cara Therapeutics (completed), with compensation paid from DCI to Tufts Medical Center, and directly to Tufts Medical Center for AstraZeneca (site PI, completed 2020), CSL Behring (site PI, ongoing), Goldfinch Bio (site PI, ongoing), and Janssen Biopharmaceuticals (site PI, completed 2019). All remaining authors have nothing to disclose.
This report was supported by DCI. C.M. Hsu receives support from ASN KidneyCure’s Ben J. Lipps Research Fellowship.
Because Dana Miskulin is an associate editor of CJASN, she was not involved in the peer review process for this manuscript. Another editor oversaw the peer review and decision-making process for this manuscript.
C.M. Hsu’s funder had no role in study design, data collection, reporting, or the decision to submit.
This article contains supplemental material online at http://cjasn.asnjournals.org/lookup/suppl/doi:10.2215/CJN.12250921/-/DCSupplemental.
Supplemental Appendix 1. Supplemental Methods.
Supplemental Table 1. Baseline patient characteristics by maximum initial titer, among those without a history of COVID-19.
Supplemental Figure 1. Kaplan–Meier time-to-event curves for the outcome of Ab titer <2 or diagnosis of COVID-19, among those without a history of COVID-19, by vaccine type.
Supplemental Figure 2. Kaplan–Meier time-to-event curves for the outcome of Ab titer <1 only, among those without a history of COVID-19, by vaccine type.
Supplemental Figure 3. Kaplan–Meier time-to-event curves for the outcome of anti-spike IgG titer <2 or diagnosis of COVID-19, among those without a history of COVID-19, by maximum initial anti-spike IgG titer.
Supplemental Figure 4. Kaplan–Meier time-to-event curves for the outcome of anti-spike IgG titer <1 only, among those without a history of COVID-19, by maximum initial anti-spike IgG titer.
Supplemental Figure 5. Multivariable Cox proportional hazards regression of clinical characteristics associated with the outcome of anti-spike IgG titer <2 or development of COVID-19.
Supplemental Figure 6. Multivariable Cox proportional hazards regression of clinical characteristics associated with the outcome of anti-spike IgG titer <1 only.
1. World Health Organization: WHO coronavirus disease (COVID-19) dashboard, 2021. Available at: https://covid19.who.int/
. Accessed September 6, 2021
2. Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Pérez Marc G, Moreira ED, Zerbini C, Bailey R, Swanson KA, Roychoudhury S, Koury K, Li P, Kalina WV, Cooper D, Frenck Jr RW, Hammitt LL, Türeci Ö, Nell H, Schaefer A, Ünal S, Tresnan DB, Mather S, Dormitzer PR, Şahin U, Jansen KU, Gruber WC; C4591001 Clinical Trial Group: Safety and efficacy of the BNT162b2 mRNA covid-19 vaccine. N Engl J Med 383: 2603–2615, 2020
3. Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB, McGettigan J, Khetan S, Segall N, Solis J, Brosz A, Fierro C, Schwartz H, Neuzil K, Corey L, Gilbert P, Janes H, Follmann D, Marovich M, Mascola J, Polakowski L, Ledgerwood J, Graham BS, Bennett H, Pajon R, Knightly C, Leav B, Deng W, Zhou H, Han S, Ivarsson M, Miller J, Zaks T; COVE Study Group: Efficacy and safety of the mRNA-1273 SARS-CoV-2
vaccine. N Engl J Med 384: 403–416, 2021
4. Sadoff J, Gray G, Vandebosch A, Cárdenas V, Shukarev G, Grinsztejn B, Goepfert PA, Truyers C, Fennema H, Spiessens B, Offergeld K, Scheper G, Taylor KL, Robb ML, Treanor J, Barouch DH, Stoddard J, Ryser MF, Marovich MA, Neuzil KM, Corey L, Cauwenberghs N, Tanner T, Hardt K, Ruiz-Guiñazú J, Le Gars M, Schuitemaker H, Van Hoof J, Struyf F, Douoguih M; ENSEMBLE Study Group: Safety and efficacy of single-dose Ad26.COV2.S vaccine against Covid-19. N Engl J Med 384: 2187–2201, 2021
5. Brosh-Nissimov T, Orenbuch-Harroch E, Chowers M, Elbaz M, Nesher L, Stein M, Maor Y, Cohen R, Hussein K, Weinberger M, Zimhony O, Chazan B, Najjar R, Zayyad H, Rahav G, Wiener-Well Y: BNT162b2 vaccine breakthrough: Clinical characteristics of 152 fully vaccinated hospitalized COVID-19 patients in Israel. Clin Microbiol Infect 27: 1652–1657, 2021
6. Tenforde MW, Patel MM, Ginde AA, Douin DJ, Talbot HK, Casey JD, Mohr NM, Zepeski A, Gaglani M, McNeal T, Ghamande S, Shapiro NI, Gibbs KW, Files DC, Hager DN, Shehu A, Prekker ME, Erickson HL, Exline MC, Gong MN, Mohamed A, Henning DJ, Peltan ID, Brown SM, Martin ET, Monto AS, Khan A, Hough CT, Busse L, Ten Lohuis CC, Duggal A, Wilson JG, Gordon AJ, Qadir N, Chang SY, Mallow C, Gershengorn HB, Babcock HM, Kwon JH, Halasa N, Chappell JD, Lauring AS, Grijalva CG, Rice TW, Jones ID, Stubblefield WB, Baughman A, Womack KN, Lindsell CJ, Hart KW, Zhu Y, Olson SM, Stephenson M, Schrag SJ, Kobayashi M, Verani JR, Self WH: Effectiveness of SARS-CoV-2
mRNA vaccines for preventing Covid-19 hospitalizations in the United States. Clin Infect Dis, 2021 34358310
7. US Department of Health and Human Services, Centers for Disease Control and Prevention: Media statement from CDC Director Rochelle P. Walensky, MD, MPH, on signing the advisory committee on immunization practices’ recommendation for an additional dose of an mRNA COVID-19 vaccine in moderately to severely immunocompromised people, 2021. Available at: https://www.cdc.gov/media/releases/2021/s0813-additional-mRNA-mrna-dose.html
. Accessed August 30, 2021
8. Centers for Disease Control and Prevention: COVID-19 vaccine booster shots, 2021. Available at: https://www.cdc.gov/coronavirus/2019-ncov/vaccines/booster-shot.html
. Accessed November 15, 2021
9. Carr EJ, Kronbichler A, Graham-Brown M, Abra G, Argyropoulos C, Harper L, Lerma EV, Suri RS, Topf J, Willicombe M, Hiremath S: Review of early immune response to SARS-CoV-2
vaccination among patients with CKD. Kidney Int Rep 6: 2292–2304, 2021
10. Lacson Jr E, Argyropoulos CP, Manley HJ, Aweh G, Chin AI, Salman LH, Hsu CM, Johnson DS, Weiner DE: Immunogenicity of SARS-CoV-2
vaccine in dialysis. J Am Soc Nephrol 32: 2735–2742, 2021
11. Longlune N, Nogier MB, Miedougé M, Gabilan C, Cartou C, Seigneuric B, Del Bello A, Marion O, Faguer S, Izopet J, Kamar N: High immunogenicity of a messenger RNA-based vaccine against SARS-CoV-2
in chronic dialysis patients. Nephrol Dial Transplant 36: 1704–1709, 2021
12. Anand S, Montez-Rath ME, Han J, Garcia P, Cadden L, Hunsader P, Kerschmann R, Beyer P, Dittrich M, Block GA, Boyd SD, Parsonnet J, Chertow GM: Antibody response to COVID-19 vaccination in patients receiving dialysis. J Am Soc Nephrol 32: 2435–2438, 2021
13. Agur T, Ben-Dor N, Goldman S, Lichtenberg S, Herman-Edelstein M, Yahav D, Rozen-Zvi B, Zingerman B: Antibody response to mRNA SARS-CoV-2
vaccine among dialysis patients - A prospective cohort study. Nephrol Dial Transplant 36: 1347–1349, 2021
14. Chan L, Fuca N, Zeldis E, Campbell KN, Shaikh A: Antibody response to mRNA-1273 SARS-CoV-2
vaccine in hemodialysis patients with and without prior COVID-19. Clin J Am Soc Nephrol 16: 1258–1260, 2021
15. Labriola L, Scohy A, Van Regemorter E, Robert A, Clerbaux G, Gillerot G, Pochet JM, Biller P, De Schuiteneer M, Morelle J, Yombi JC, Kabamba B, Rodriguez-Villalobos H, Jadoul M: Immunogenicity of BNT162b2 SARS-CoV-2
vaccine in a multicenter cohort of nursing home residents receiving maintenance hemodialysis. Am J Kidney Dis 78: 766–768, 2021
16. Danthu C, Hantz S, Dahlem A, Duval M, Ba B, Guibbert M, El Ouafi Z, Ponsard S, Berrahal I, Achard JM, Bocquentin F, Allot V, Rerolle JP, Alain S, Touré F: Humoral response after SARS-CoV-2
mRNA vaccination in a cohort of hemodialysis patients and kidney transplant recipients. J Am Soc Nephrol 32: 2153–2158, 2021
17. Chi C, Patel P, Pilishvili T, Moore M, Murphy T, Strikas R: Guidelines for vaccinating kidney dialysis patients and patients with chronic kidney disease, Atlanta, GA, Centers for Disease Control and Prevention, 2012. Available at: https://www.cdc.gov/dialysis/pdfs/vaccinating_dialysis_patients_and_patients_dec2012.pdf
. Accessed August 30, 2021
18. Mizrahi B, Lotan R, Kalkstein N, Peretz A, Perez G, Ben-Tov A, Chodick G, Gazit S, Patalon T: Correlation of SARS-CoV-2
-breakthrough infections to time-from-vaccine. Nat Commun 12: 6379, 2021
19. Bergwerk M, Gonen T, Lustig Y, Amit S, Lipsitch M, Cohen C, Mandelboim M, Levin EG, Rubin C, Indenbaum V, Tal I, Zavitan M, Zuckerman N, Bar-Chaim A, Kreiss Y, Regev-Yochay G: Covid-19 breakthrough infections in vaccinated health care workers. N Engl J Med 385: 1474–1484, 2021
20. Chung EYM, Palmer SC, Natale P, Krishnan A, Cooper TE, Saglimbene VM, Ruospo M, Au E, Jayanti S, Liang A, Jie Deng DJ, Chui J, Higgins GY, Tong A, Wong G, Teixeira-Pinto A, Hodson EM, Craig JC, Strippoli GFM: Incidence and outcomes of COVID-19 in people with CKD: A systematic review and meta-analysis. Am J Kidney Dis 78: 804–815, 2021
21. Hsu CM, Weiner DE, Aweh G, Miskulin DC, Manley HJ, Stewart C, Ladik V, Hosford J, Lacson EC, Johnson DS, Lacson Jr E: COVID-19 among US dialysis patients: Risk factors and outcomes from a national dialysis provider. Am J Kidney Dis 77: 748–756.e1, 2021
22. SIEMENS: COV2G, ADVIA Centaur XP and ADVIA Centaur XPT Systems, 2020. Available at: https://www.fda.gov/media/140704/download
. Accessed June 22, 2021
23. Centers for Disease Control and Prevention: COVID-19: When you’ve been fully vaccinated, 2021. Available at: https://www.cdc.gov/coronavirus/2019-ncov/vaccines/fully-vaccinated.html
. Accessed July 20, 2021
24. Espi M, Charmetant X, Barba T, et al. A prospective observational study for justification, safety, and efficacy of a third dose of mRNA vaccine in patients receiving maintenance hemodialysis. Kidney Int
. 101: 390–402, 2022
25. Pegu A, O'Connell SE, Schmidt SD, O'Dell S, Talana CA, Lai L, Albert J, Anderson E, Bennett H, Corbett KS, Flach B, Jackson L, Leav B, Ledgerwood JE, Luke CJ, Makowski M, Nason MC, Roberts PC, Roederer M, Rebolledo PA, Rostad CA, Rouphael NG, Shi W, Wang L, Widge AT, Yang ES, Beigel JH, Graham BS, Mascola JR, Suthar MS, McDermott AB, Doria-Rose NA, Arega J, Beigel JH, Buchanan W, Elsafy M, Hoang B, Lampley R, Kolhekar A, Koo H, Luke C, Makhene M, Nayak S, Pikaart-Tautges R, Roberts PC, Russell J, Sindall E, Albert J, Kunwar P, Makowski M, Anderson EJ, Bechnak A, Bower M, Camacho-Gonzalez AF, Collins M, Drobeniuc A, Edara VV, Edupuganti S, Floyd K, Gibson T, Ackerley CMG, Johnson B, Kamidani S, Kao C, Kelley C, Lai L, Macenczak H, McCullough MP, Peters E, Phadke VK, Rebolledo PA, Rostad CA, Rouphael N, Scherer E, Sherman A, Stephens K, Suthar MS, Teherani M, Traenkner J, Winston J, Yildirim I, Barr L, Benoit J, Carste B, Choe J, Dunstan M, Erolin R, Ffitch J, Fields C, Jackson LA, Kiniry E, Lasicka S, Lee S, Nguyen M, Pimienta S, Suyehira J, Witte M, Bennett H, Altaras NE, Carfi A, Hurley M, Leav B, Pajon R, Sun W, Zaks T, Coler RN, Larsen SE, Neuzil KM, Lindesmith LC, Martinez DR, Munt J, Mallory M, Edwards C, Baric RS, Berkowitz NM, Boritz EA, Carlton K, Corbett KS, Costner P, Creanga A, Doria-Rose NA, Douek DC, Flach B, Gaudinski M, Gordon I, Graham BS, Holman L, Ledgerwood JE, Leung K, Lin BC, Louder MK, Mascola JR, McDermott AB, Morabito KM, Novik L, O'Connell S, O'Dell S, Padilla M, Pegu A, Schmidt SD, Shi W, Swanson PA, Talana CA, Wang L, Widge AT, Yang ES, Zhang Y, Chappell JD, Denison MR, Hughes T, Lu X, Pruijssers AJ, Stevens LJ, Posavad CM, Gale M, Menachery V, Shi P-Y: Durability of mRNA–1273 vaccine-induced antibodies against SARS-CoV-2
variants. Science 373: 1372–1377, 2021
26. Doria-Rose N, Suthar MS, Makowski M, O’Connell S, McDermott AB, Flach B, Ledgerwood JE, Mascola JR, Graham BS, Lin BC, O’Dell S, Schmidt SD, Widge AT, Edara VV, Anderson EJ, Lai L, Floyd K, Rouphael NG, Zarnitsyna V, Roberts PC, Makhene M, Buchanan W, Luke CJ, Beigel JH, Jackson LA, Neuzil KM, Bennett H, Leav B, Albert J, Kunwar P; mRNA-1273 Study Group: Antibody persistence through 6 months after the second dose of mRNA-1273 vaccine for Covid-19. N Engl J Med 384: 2259–2261, 2021
27. Barouch DH, Stephenson KE, Sadoff J, Yu J, Chang A, Gebre M, McMahan K, Liu J, Chandrashekar A, Patel S, Le Gars M, de Groot AM, Heerwegh D, Struyf F, Douoguih M, van Hoof J, Schuitemaker H: Durable humoral and cellular immune responses following Ad26.COV2.S vaccination for COVID-19. N Engl J Med 385: 951–953, 2021
28. Favresse J, Bayart JL, Mullier F, Elsen M, Eucher C, Van Eeckhoudt S, Roy T, Wieers G, Laurent C, Dogné JM, Closset M, Douxfils J: Antibody titres decline 3-month post-vaccination with BNT162b2. Emerg Microbes Infect 10: 1495–1498, 2021
29. Naaber P, Tserel L, Kangro K, Sepp E, Jürjenson V, Adamson A, Haljasmägi L, Rumm AP, Maruste R, Kärner J, Gerhold JM, Planken A, Ustav M, Kisand K, Peterson P: Dynamics of antibody response to BNT162b2 vaccine after six months: A longitudinal prospective study. Lancet Reg Health Eur 10: 100208, 2021
30. Levin EG, Lustig Y, Cohen C, Fluss R, Indenbaum V, Amit S, Doolman R, Asraf K, Mendelson E, Ziv A, Rubin C, Freedman L, Kreiss Y, Regev-Yochay G: Waning immune humoral response to BNT162b2 Covid-19 vaccine over 6 months. N Engl J Med 385: e84, 2021
31. Wei J, Stoesser N, Matthews PC, Ayoubkhani D, Studley R, Bell I, Bell JI, Newton JN, Farrar J, Diamond I, Rourke E, Howarth A, Marsden BD, Hoosdally S, Jones EY, Stuart DI, Crook DW, Peto TEA, Pouwels KB, Eyre DW, Walker AS; COVID-19 Infection Survey team: Antibody responses to SARS-CoV-2
vaccines in 45,965 adults from the general population of the United Kingdom. Nat Microbiol 6: 1140–1149, 2021
32. Earle KA, Ambrosino DM, Fiore-Gartland A, Goldblatt D, Gilbert PB, Siber GR, Dull P, Plotkin SA: Evidence for antibody as a protective correlate for COVID-19 vaccines. Vaccine 39: 4423–4428, 2021
33. Harris RJ, Hall JA, Zaidi A, Andrews NJ, Dunbar JK, Dabrera G: Effect of vaccination on household transmission of SARS-CoV-2
in England. N Engl J Med 385: 759–760, 2021
34. Dekervel M, Henry N, Torreggiani M, Pouteau LM, Imiela JP, Mellaza C, Garnier AS, Dujardin A, Asfar M, Ducancelle A, Paquin A, Blanchi S, Besson V, Piccoli GB, Augusto JF: Humoral response to a third injection of BNT162b2 vaccine in patients on maintenance haemodialysis. Clin Kidney J 14: 2349–2355, 2021
35. Ducloux D, Colladant M, Chabannes M, Yannaraki M, Courivaud C: Humoral response after 3 doses of the BNT162b2 mRNA COVID-19 vaccine in patients on hemodialysis. Kidney Int 100: 702–704, 2021
36. Bensouna I, Caudwell V, Kubab S, Acquaviva S, Pardon A, Vittoz N, Bozman DF, Hanafi L, Faucon AL, Housset P: SARS-CoV-2
antibody response after a third dose of the BNT162b2 vaccine in patients receiving maintenance hemodialysis or peritoneal dialysis [published online ahead of print September 8, 2021]. Am J Kidney Dis 10.1053/j.ajkd.2021.08.005
37. Centers for Disease Control and Prevention: Summary document for interim clinical considerations for use of COVID-19 vaccines currently authorized in the United States, 2021. Available at: https://www.cdc.gov/vaccines/covid-19/downloads/summary-interim-clinical-considerations.pdf
. Accessed August 31, 2021
38. Hsu CM, Weiner DE, Aweh GN, Manley HJ, Ladik V, Frament J, Miskulin D, Argyropoulos C, Abreo K, Chin A, Gladish R, Salman L, Johnson D, Lacson EK: Seroresponse to SARS-CoV-2
vaccines among maintenance dialysis patients [published online ahead of print November 7, 2021]. Am J Kidney Dis 10.1053/j.ajkd.2021.10.002
39. Hsu CM, Weiner DE, Aweh G, Salenger P, Johnson DS, Lacson Jr E: Epidemiology and outcomes of COVID-19 in home dialysis patients compared with in-center dialysis patients. J Am Soc Nephrol 32: 1569–1573, 2021