Introduction

Coronavirus Disease (COVID-19) pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has determined a substantial increment in morbidity and mortality worldwide [1]. Nursing home (NH) residents, that often present with a high burden of comorbidities and clinical complexities, suffered the greatest impact of the pandemic in many countries worldwide, independently of health care system organization [2,3,4,5]. Epidemiological data indicate that during the first pandemic wave, up to 50% of deaths from COVID-19 may have occurred within NH facilities [6]. For this reason, in many Western countries, priority has been given to this population to receive anti-SARS-CoV-2 vaccination. Starting from the end of December 2020, the Italian government has implemented vaccination programmes in NH to reduce the risk of COVID-19-related morbidity and mortality in this high-risk population [7]. Priority was given to the use of mRNA vaccines (mRNA-1273 or BNT162b2) in this population. Residents with no prior history of SARS-CoV-2 infection received two doses of mRNA vaccine. Vaccination was also recommended for residents with a history of prior SARS-CoV-2 infection. The Italian Ministry of Health recommended a single dose for those with a history of SARS-CoV-2 infection between 3 and 6 months beforehand and two doses for those with a history of infection more than 6 months beforehand [7].

Recent data indicate that immune response to vaccination tends to reduce over time and that this reduction is associated with breakthrough SARS-CoV-2 infections [8,9,10]. In addition, in healthy individuals, a prior SARS-CoV-2 infection was associated with a higher antibody level, suggesting that prior infection history may increase protection from vaccination and that different strategies and timing could be employed in the vaccination strategy, as well as in the administration of booster doses, in relation to the history of previous infection [11]. However, the available evidence cannot be generalized to NH residents. Limited data are available on the duration of the protection of vaccination and on the immunisation, coverage ensured by a prior infection in this population. In addition, immune response to vaccination might be reduced in frail NH residents with clinical complexity and it might be hypothesized that the potential benefits of hybrid immunity may also be decreased in this population compared to healthy individuals.

For these reasons, the present study aims to monitor antibody levels and their persistence over a 6-months period in NH residents according to the history of prior SARS-CoV-2 infection. This study is performed in the context of the GeroCovid Vax study [12], a multicentre Italian project monitoring effectiveness of SARS-CoV-2 vaccination in NH nationwide.

Methods

GeroCovid Vax study

GeroCOVID VAX study is promoted by the Italian Society of Gerontology and Geriatrics (SIGG) (Florence, Italy) and the Istituto Superiore di Sanità (ISS, Rome, Italy) and sponsored by the Italian Medicines Agency (AIFA). The study began in February 2021 and aimed at investigating the effects of anti-SARS-CoV-2 vaccine use in older NH residents in Italy [12]. Residents were consecutively enrolled within the vaccination calendar scheduled in each participating NH. The delay with respect to the formal start of the vaccination campaign had no impact on the representativeness of the study sample as the vaccination become fully operational in the first quarter of 2021. Main GeroCovid Vax study objectives include: (i) evaluating he efficacy and safety of the SARS-CoV-2 vaccine in a representative sample of older NH residents, and (ii) evaluate humoral and cellular immune response in a large subpopulation of study participants. The inclusion criteria were age ≥ 60 years, life expectancy ≥ 3 months, expected NH stay ≥ 3 months, receiving at least one dose of any type of anti-SARS-CoV-2 vaccine. Demographic and clinical data were collected by trained researchers at study enrolment (prior to the first dose of vaccine). These included age, sex, chronic diseases, and history of confirmed SARS-CoV-2 infection (as assessed by reverse transcriptase–polymerase chain reaction testing). Humoral immune response was evaluated in a sample of 395 residents at study enrolment (prior to the first dose of vaccine, T0) and then 2 (T1) and 6 months (T2) following the first vaccine dose.

Serum preparation and storage

All blood samples were properly prepared and stored following a standardized procedure. Blood samples were collected in Serum Separator Tubes (BD Diagnostic Systems, Franklin Lakes, NJ, USA) and centrifuged at room temperature at 1600 rpm for 10 min. Aliquots were transferred to 2 ml polypropylene screw cap cryotubes (Nunc™, Thermofisher Scientific, Waltham, MA USA) and immediately frozen at -20 °C. Frozen sera were then shipped to the ISS as a national reference laboratory for COVID-19, in dry ice following biosafety shipment condition. Upon arrival serum samples were immediately stored at − 80 °C.

SARS-CoV-2 IgG immunoassays

The Liaison® SARS-CoV-2 TrimericS IgG chemiluminescent assay (DiaSorin, Italy), using the trimeric S antigen stabilized in its native form and designed for high throughput in healthcare settings was used. The LIAISON® XL fully automated chemiluminescence analyzer automatically calculates SARS-CoV-2 trimeric S IgG antibody concentrations, expressed as binding antibody units (BAU/ml). The assay range is up to 2080 BAU/ml. According to the manufacturer’s instructions, values ≥ 33.8 BAU/ml were interpreted as positive. Samples that were above the upper limit of the assay were automatically diluted 1:20 and re-analysed.

Statistical analysis

Baseline characteristics according to prior SARS-CoV-2 infection were compared using analysis of variance (ANOVA) for normally distributed variables, nonparametric Kruskal–Wallis H tests for skewed variables and chi-square analyses for dichotomous variables. Given the non-normal distribution of SARS-CoV-2 trimeric S IgG antibody concentrations, analyses were performed using log-transformed values and geometric means were calculated (GM). Analysis of covariance (ANCOVA) was used to compare means of SARS-CoV-2 trimeric S IgG antibody concentrations according to prior SARS-CoV-2 infection. Among residents with prior SARS-CoV-2 infection antibody concentration according to number of doses received (1 vs. 2 doses) and time from SARS-CoV-2 infection (≤ 4 months vs. ≥ 5 months) was calculated. To avoid the confounding effect related to the number of vaccine doses received, the effect of time from SARS-CoV-2 infection on antibody concentration was analysed only in residents receiving a single vaccine dose. Variables considered for adjustment in the ANCOVA models were age, sex and those associated with prior SARS-CoV-2 infection at p ≤ 0.10 at the univariate analysis. Statistical analysis was carried out with STATA Software Version 16.1 (Stata Cooperation, College Station, TX, USA).

Ethical approval

The study was approved by the Italian National Ethical Committee with permission number 264/2021 (January 26, 2021).

Results

Study sample

The study sample consisted of 395 residents from 25 NHs in 6 Italian Regions. Table 1 shows resident’s characteristics according to prior SARS-CoV-2 infection. Mean age of the study sample was 82.4 ± 9.5 years and 68% of residents were women. Most residents received BNT162b2 vaccine (87%). Dementia was the most common condition observed (54% of residents), followed by hypertension (50%), ischemic heart diseases (29%), diabetes (16%) and chronic obstructive pulmonary disease (16%). Overall, 139 residents (35.2%) had SARS-CoV-2 infection prior to study enrolment. As compared with residents with prior SARS-CoV-2 infection, those without infection were older and had a significantly higher prevalence of chronic renal failure. Among the 139 residents with prior SARS-CoV-2 infection, 118 (85%) received a single vaccine dose and 21 (15%) two doses. Among the 118 residents receiving a single dose of vaccine, 80 (67.8%) had prior infection ≤ 4 months before vaccination, 33 (28.0%) ≥ 5 months before vaccination and in 5 (4.2%) residents the information on SARS-CoV-2 infection date was not available.

Table 1 Demographic and clinical characteristics of the study sample
Full size table

SARS-CoV-2 trimeric S IgG antibody concentration and prior-SARS-CoV-2 infection

Figure 1 shows SARS-CoV-2 trimeric S IgG antibody concentration before vaccination (T0), 2 months (T1) and 6 months (T2) after the first dose according to prior SARS-CoV-2 infection. Significantly higher antibody levels were present at T0 in residents with prior SARS-CoV-2 infection. Antibody concentration reached the highest level 2 months after vaccination (T1) and then declined at 6 months (T2).

Fig. 1
figure 1

SARS-CoV-2 trimeric S IgG antibody concentration (log-transformed values) before vaccination (T0), 2 months (T1) and 6 months (T2) after first dose of vaccine according to prior SARS-CoV-2 infection. Data are presented for the whole sample (upper panel, n = 395), for BNT162b2 (n = 344, lower left panel), and mRNA-1273 vaccines (n = 51 lower right panel)

Full size image

Overall, 392 (99%) residents at 2 months (T1) and 343 (87%) at 6 months after vaccination (T2) had an antibody concentration above the 33.8 BAU/ml threshold. The response to vaccination was significantly higher in residents with prior SARS-CoV-2 infection who continued to have significantly higher antibody levels at 2- (T1) and 6-month (T2) follow-ups. When data were stratified according to the type of vaccine, we found that the effect of prior SARS-CoV-2 infection on antibody concentration was consistent for both mRNA-1273 and BNT162b2 vaccines. We did not observe any significant impact of any of the conditions suffered by residents reported on the antibody response to vaccination.

Table 2 shows adjusted GM (Standard Errors) of SARS-CoV-2 trimeric S IgG antibody concentration among participating residents, according to prior SARS-CoV-2 infection. Participants with a prior infection presented a significant higher concentration of antibodies than those without a history of infection before vaccination (T0; GM 186.6 vs. 6.1 BAU/ml, p < 0.001) and at the 2- (T1; GM 5264.1 vs. 944.4 BAU/ml, p < 0.001) and 6-month (T2; GM 1473.6 vs. 128.7 BAU/ml, p < 0.001) follow-ups. This association was consistent in both users of mRNA-1273 or BNT162b2. Independently of prior SARS-CoV-2 infection, residents receiving mRNA-1273 had significantly higher antibody concentration than those receiving BNT162b2.

Table 2 Geometric means (Standard Errors) of Anti-S IgG (BAU/mL), according to prior SARS-CoV-2 infection, at baseline assessment (before vaccination—T0), 2 months (T1) and 6 months (T2) after first dose of vaccine
Full size table

SARS-CoV-2 trimeric S IgG antibody concentration in residents with prior-SARS-CoV-2 infection

Table 3 shows geometric means of SARS-CoV-2 trimeric S IgG antibody concentration in residents with prior SARS-CoV-2 infection according to number of doses received and time of SARS-CoV-2 infection diagnosis. Residents with prior SARS-CoV-2 infection receiving two vaccine doses presented significantly higher antibody concentration in the 2- and 6-month follow-ups (T1 and T2). Independently of the number of doses received, residents with prior SARS-CoV-2 infection had higher antibody concentration at 2- and 6-month follow-ups than those with no SARS-CoV-2 infection history. To avoid the confounding effect related to the number of vaccine doses received, the effect of time from SARS-CoV-2 infection on antibody concentration was analysed only in residents receiving a single vaccine dose. As shown in Table 3, residents experiencing SARS-CoV-2 infection ≥ 5 months before vaccination had a lower level of antibody concentration before vaccination (T0), but this association was reversed after vaccination. At the 2- and 6-month follow-ups (T1 and T2), this group presented a significantly higher antibody concentration as compared with residents experiencing SARS-CoV-2 infection ≤ 4 months before vaccination. The multiplicative factor of a previous infection on the antibody response induced by vaccination was 11.4 at the T2 follow-up. More in detail, SARS-CoV-2 trimeric S IgG antibody concentration after a single vaccine dose, was 16.1-fold higher in residents who had the previous infection ≥ 5 months before vaccination and 7.3-fold higher in residents who had SARS-CoV-2 infection ≤ 4 months before vaccination.

Table 3 Geometric means (Standard Errors) of Anti-S IgG (BAU/mL) in residents with Prior SARS-CoV-2 infection at baseline assessment (before vaccination—T0), 2 months (T1) and 6 months (T2) after the first dose of vaccine according to number of doses received and months from SARS-CoV-2 infection
Full size table

Discussion

Frail NH residents suffered the most severe consequences from SARS-CoV-2 epidemic. For this reason, particular attention to the effect of prevention strategies on this population is a priority to limit the impact of the epidemic worldwide. The main finding of the present study is that significantly superior humoral immunity is induced by mRNA vaccines in NH residents with a previous SARS-CoV-2 infection compared to residents without prior infection.

Overall, the administration of SARS-CoV-2 mRNA vaccines resulted immunogenic in NH residents. Indeed, two months after the completion of the primary vaccine schedule, almost 100% of the residents showed a positive anti-trimeric Spike IgG titer. Six months after the first immunization still more than 85% of residents had a titer above the positivity cut-off of the serological assay used, an observation that extends to older adults living in NH findings results obtained in other settings and age-groups [8,9,10,11]. The number of vaccine doses influenced the antibody response. A longer interval between SARS-CoV-2 infection and vaccination was associated with a better humoral immune response.

It has been shown that in subjects previously infected by SARS-CoV-2, vaccination increased all humoral response components [13]. The potentiating effect of a previous infection is not surprising and could be attributed to the so-called hybrid immunity [14]. Immunological memory generated after exposure to SARS-CoV-2 is promptly activated by subsequent vaccine immunization, leading to an enhanced immune response [14].

The hybrid immunity effect on the magnitude of vaccine-induced humoral response has been shown in several studies. Among vaccinated health care workers from the UK, previously infected individuals expressed higher levels of anti-SARS-CoV-2 IgG than those with no previous SARS-CoV-2 infection after a single dose of BNT162b2 [

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Acknowledgements

List of GeroCovid Vax Study Group researcher is available at ‘Abbatecola A, Antonelli Incalzi R, Malara A, Palmieri A, Di Lonardo A, Borselli G, Russo M, Noale M, Fumagalli S, Gareri P, Mossello E, Trevisan C, Volpato S, Monzani F, Coin A, Bellelli G, Okoye C, del Signore S, Zia G, & GeroCovid Vax Group. Disentangling the impact of COVID-19 infection on clinical outcomes and preventive strategies in older persons: an Italian perspective. Journal of Gerontology and Geriatrics. 2021 1-9. https://doi.org/10.36150/2499-6564-N440.’ (Ref. 12). We gratefully acknowledge the technical assistance of Daniela Diamanti and Fabiola Diamanti.

Funding

The GeroCovid Vax Study was funded by a grant from the Italian Medicines Agency (Agenzia Italiana del Farmaco, AIFA – resolution n 14 – feb 4, 2021).

Author information

Author notes

  1. Giorgio Fedele and Annapina Palmieri equally contributed to this work as Co-first authors.

  2. Paola Stefanelli and Graziano Onder equally contributed to this work as Co-Last authors.

Authors and Affiliations

  1. VPD, Reference Labs Unit, Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy

    Giorgio Fedele, Pasqualina Leone, Ilaria Schiavoni, Anna Teresa Palamara & Paola Stefanelli

  2. Department of Cardiovascular, Endocrine-Metabolic Diseases and Aging, Istituto Superiore di Sanità, Rome, Italy

    Annapina Palmieri, Cecilia Damiano, Anna Di Lonardo & Graziano Onder

  3. Department of Medical Sciences, University of Ferrara, Ferrara, Italy

    Caterina Trevisan

  4. Alzheimer’s Disease Day Clinic Department, Azienda Sanitaria Locale, Frosinone, Italy

    Angela Marie Abbatecola

  5. Geriatrics Outpatient Clinic and Territorial Residences, Italian Hospital Group, Rome, Italy

    Carmine Cafariello

  6. ANASTE Humanitas Foundation, Rome, Italy

    Alba Malara

  7. Department of Microbiology and Virology, Pugliese Ciaccio Hospital, Catanzaro, Italy

    Pasquale Minchella & Giuseppina Panduri

  8. Geriatrics Unit, Department of Medicine, Campus Bio-Medico University and Teaching Hospital, Rome, Italy

    Raffaele Antonelli Incalzi

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  1. Giorgio Fedele
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The GeroCovid Vax Study Group

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Correspondence to Giorgio Fedele.

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The study was conducted in accordance with Helsinki declaration as revised in 2013.

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Fedele, G., Palmieri, A., Damiano, C. et al. Humoral immunity induced by mRNA COVID-19 vaccines in Nursing Home Residents previously infected with SARS-CoV-2. Aging Clin Exp Res 34, 2577–2584 (2022). https://doi.org/10.1007/s40520-022-02239-0

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