High viral loads: what drives fatal cases of COVID-19 in vaccinees? – an autopsy study

Twenty-nine consecutively collected cases were analyzed and compared to 141 nonvaccinated control cases. Autopsies were performed on 16 partially and 13 fully vaccinated individuals. Most patients were elderly and suffered from several relevant comorbidities.

However, vaccinated cases also showed high viral loads, reaching Ct-values below 10, especially in the upper airways and lungs. This was accompanied by high rates of pulmonal bacterial or mycotic superinfections and the occurrence of immunocompromising factors, such as malignancies, immunosuppressive drug intake, or decreased immunoglobulin levels. All these findings were particularly accentuated in partially vaccinated patients compared to fully vaccinated individuals.

The virus dissemination observed in our case study may indicate that patients with an impaired immune system have a decreased ability to eliminate the virus. However, the potential role of antibody-dependent enhancement must also be ruled out in future studies. Fatal cases of COVID-19 in vaccinees were rare and often associated with severe comorbidities or other immunosuppressive conditions.

Abstract

The rate of SARS-CoV-2 infections in vaccinees has become a relevant serious issue. This study aimed to determine the causes of death, histological organ alteration, and viral spread in relation to demographic, clinical-pathological, viral variants, and vaccine types for deceased individuals with proven SARS-CoV-2 infection after vaccination who died between January and November 2021. Twenty-nine consecutively collected cases were analyzed and compared to 141 nonvaccinated control cases. Autopsies were performed on 16 partially and 13 fully vaccinated individuals. Most patients were elderly and suffered from several relevant comorbidities. Real-time RT-PCR (RT-qPCR) identified a significantly increased rate of generalized viral dissemination within organ systems in vaccinated cases versus nonvaccinated cases (45% vs. 16%, respectively; P = 0.008) mainly with Ct-values of higher than 25 in non-respiratory samples. However, vaccinated cases also showed high viral loads, reaching Ct-values below 10, especially in the upper airways and lungs. This was accompanied by high rates of pulmonal bacterial or mycotic superinfections and the occurrence of immunocompromising factors, such as malignancies, immunosuppressive drug intake, or decreased immunoglobulin levels. All these findings were particularly accentuated in partially vaccinated patients compared to fully vaccinated individuals. The virus dissemination observed in our case study may indicate that patients with an impaired immune system have a decreased ability to eliminate the virus. However, the potential role of antibody-dependent enhancement must also be ruled out in future studies. Fatal cases of COVID-19 in vaccinees were rare and often associated with severe comorbidities or other immunosuppressive conditions.

Results

Representativity of the cohort

Given the 303 cases of deceased individuals with COVID-19 during the time of vaccine availability in the Augsburg Center, the 42 (14%) deceased individuals with COVID-19 after vaccination, 23 of which (autopsy rate 55%) are included in this study, indicates that the study cohort is representative.

The University Medical Center Augsburg is the only tertiary medical center in a region with about two million inhabitants. For the city of Augsburg, the rate of completely vaccinated persons is 65% (194,000 persons; status: 4 November 2021)40. The 16 deceased cases after full vaccination represent a rate of 0.008%, which is considerably low and in line with a large population-based study carried out in Scotland showing a rate of 0.007% 41.

Partially vaccinated cases

Partial vaccination was present in 16 cases. The median time between vaccination and the first positive PCR test was 10 days (range: 1–24). Eleven patients received the BNT162b2 vaccine (BioNTech), and four were vaccinated with AZD1222 (AstraZeneca). In one case, information regarding the vaccine was not available. There was a nonsignificant trend toward the predominance of females among AZD1222 vaccinated patients (P = 0.282). Otherwise, the female and male genders were balanced in this group. No correlation was found between the vaccine and other clinical-pathological data. The viral variants included five cases of non-VOCs (B.1.221, B.1.258, B.1.9.4) and 11 VOCs (ten alpha, one delta; see Table 1, Supplementary Table 1 and Fig. 4 for lineage assignment). This finding reflected the prevalent variants at the respective times of the pandemic (Figs. 2 and 4).

In one case (C6), the SARS-CoV-2 infection was most likely not the cause of death, according to the definition of the WHO. This patient died due to traumatic cerebral bleeding. In the remaining 15 cases, the underlying cause of death based on the WHO definition33 was COVID-19. The direct cause of death in three of the 15 cases was cerebral ischemia, cardiac failure, and bleeding, while 12 patients died directly due to severe COVID-19 pneumonia with diffuse alveolar damage (DAD) (Table 1 and Supplementary Table 1). The histological presentation of the cases especially also of the lungs was similar to that of nonvaccinated cases (Fig. 3). RT-qPCR-based detection of SARS-CoV-2 RNA from upper airway swabs revealed low Ct-values (median: 18; range: 9–30), indicating high viral loads. Intraindividual viral dissemination was identified in 11 out of 16 cases (Fig. 4B). This rate was higher than in fully vaccinated cases, with a rate of 38% (P = 0.144), but it failed to achieve significance. However, it was significantly higher compared to the 19 previously published nonvaccinated cases of the first wave17, with 16% (P = 0.002) showing such a dissemination pattern.

figure 3
Fig. 3: Representative gross and histology images.
figure 4
Fig. 4: SARS-CoV-2 lineages and viral load data on a case basis.

In partially vaccinated patients, the lungs were the most affected organs. High viral loads could be detected by RT-qPCR, with a median Ct-value of 21 (range: 14–31), confirmed by RNA-ISH (Fig. 3), which showed a strong correlation with the Ct-values (R = 0.819, P < 0.0001) in a semiquantitative analysis (Fig. 4). Another remarkable observation in this collection was the high rate of malignancies in their medical history of 56%. Again, this is considerably higher compared to the completely vaccinated cases (3 vs. 10, 23%; P = 0.130) and the naïve control cohort (30 vs. 112, 21%; P = 0.005).

Fully vaccinated cases

This study comprised 13 fully vaccinated cases. The median time from the last vaccination to a positive test of SARS-CoV-2 was 140 days (range: 28–283). The vaccines applied in the study groups were BNT162b2 (BioNTech) in 11 cases and AZD1222 (AstraZeneca) and CoronaVac (Sinovac) in one case each. The gender ratio was balanced. No correlation between vaccine type and other clinical findings was observed. SARS-CoV-2 VOCs alpha and delta were the only viral variants present (Table 1 and Supplementary Table 2 and Figs. 2 and 4).

According to the WHO classification33, all but one patient died due to COVID-19. The non-COVID-19 patient suffered from myocardial infarction and renal abscesses. The SARS-CoV-2 RT-qPCR during routine testing on admission was positive, with a very high Ct-value of 41. The condition leading directly to death, (not following the definition of the WHO), was other than COVID-19 (Table 1 and Supplementary Table 2, Fig. 1) at a rate of 31% (4 of 13). The corresponding rates were 25% (4 of 16; P = 1.000) and 8% (11 of 141; P = 0.029) in partially vaccinated cases and nonvaccinated cases, respectively.

The type of infection (“real breakthrough” versus “vaccination failure,” according to Schieffelin et al.7) could be classified in 11 of the 13 cases in which serology for SARS-CoV-2 spike-specific antibodies was positive. Five of these cases revealed high anti-spike titers (>2500 U/ml), while others showed only moderate levels (154–407 U/ml). In the remaining two cases, no antibodies against the spike protein were detected (Table 1 and Supplementary Table 2). According to these results, eight cases were classified as breakthrough infections, whereas two cases represented vaccine failures. In one case, only an asymptomatic infection was obtained. The SARS-CoV-2 nucleocapsid antibody serology revealed negative results (COI < 1) in six of 11 cases, which correlated significantly with the occurrence of viral dissemination (P = 0.015).

In contrast to the partially vaccinated cases, the viral spread in fully vaccinated cases was restricted to the upper airways and lungs in eight of the 13 cases, whereas viral dissemination throughout the organ system was seen in five cases. Again, histological changes in the organs were similar to nonvaccinated cases, with relevant impairment of the lungs. The median RT-qPCR Ct-value of the lungs was 23 (range: 17–27), similar to the partially vaccinated cases (median 21, range 14–31).

RNA-ISH from non-respiratory samples

RNA-ISH from 23 non respiratory samples (Supplementary Table 3) revealed positive results in only five samples. Positive signals were restricted to 1–4 single cells which are very likely histiocytic cells (Fig. 3I). Epithelial cells or soft tissue cells were not infected. There was a significant correlation between the Ct-values and the corresponding RNA-signal (Correlation: −0.453; P = 0.03).

RT-PCR from blood serum samples

To address the question of a potential role of viremia, seven blood serum samples which were collected 48 h maximum before death were analyzed for SARS-CoV-2-RNA by RT-PCR (Fig. 4B). Positivity with a Ct-value of 30 was found only in one case (C25) that was classified as non-disseminated. Here, an exceptionally low Ct-value in the nasopharyngeal smear was noticeable and a short time between the first positive PCR-test and the death of 6 days indicating an early phase of the disease with high viral replication.

Sequence analysis

Whole-genome sequencing was conducted for all cases with sample material having proper Ct-values, except C6, C11, C13, C14, C16, C23, C26, C29. In most cases, one sample was subjected to sequencing. For some cases, we could investigate several samples: C1 (n = 4), C17 (n = 2), C18 (n = 2), C19 (n = 2), C25 (n = 2). Sequences of corresponding samples were identical to each other.

https://www.nature.com/articles/s41379-022-01069-9

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