Occurrence of SARS-CoV-2 antibodies in an incredible nationwide sample of patients on dialysis in the United States: a negative-sectional belief – The Lancet

Abstract

Background

Many patients receiving dialysis in the United States part the socioeconomic characteristics of underserved communities, and undergo routine monthly laboratory checking out, facilitating a challenging, honest, and repeatable review of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) seroprevalence.

Ideas

For this negative-sectional belief, in partnership with a central laboratory that receives samples from approximately 1300 dialysis amenities across the United States, we examined the leisure plasma of 28 503 randomly chosen grownup patients receiving dialysis in July, 2020, utilizing a spike protein receptor binding domain complete antibody chemiluminescence assay (100% sensitivity, 99·8% specificity). We extracted records on age, sex, elope and ethnicity, and build and facility ZIP codes from the anonymised electronic health records, linking affected person-level build records with cumulative and on every day basis cases and deaths per 100 000 inhabitants and with nasal swab test positivity rates. We standardised incidence estimates per the total US dialysis and grownup inhabitants, and present estimates for four prespecified strata (age, sex, internet site, and elope and ethnicity).

Findings

The sampled inhabitants had the same age, sex, and elope and ethnicity distribution to the US dialysis inhabitants, with an even bigger percentage of older people, males, and people dwelling in majority Shadowy and Hispanic neighbourhoods than in the US grownup inhabitants. Seroprevalence of SARS-CoV-2 was once 8·0% (95% CI 7·7–8·4) in the sample, 8·3% (8·0–8·6) when standardised to the US dialysis inhabitants, and 9·3% (8·8–9·9) when standardised to the US grownup inhabitants. When standardised to the US dialysis inhabitants, seroprevalence ranged from 3·5% (3·1–3·9) in the west to 27·2% (25·9–28·5) in the northeast. Evaluating seroprevalent and case counts per 100 000 inhabitants, we discovered that 9·2% (8·7–9·8) of seropositive patients had been diagnosed. When in contrast with assorted measures of SARS-CoV-2 spread, seroprevalence correlated most effective with deaths per 100 000 inhabitants (Spearman’s ρ=0·77). Residents of non-Hispanic Shadowy and Hispanic neighbourhoods experienced bigger odds of seropositivity (odds ratio 3·9 [95% CI 3·4–4·6] and a few·3 [1·9–2·6], respectively) in contrast with residents of predominantly non-Hispanic white neighbourhoods. Residents of neighbourhoods in the final discover inhabitants density quintile experienced increased odds of seropositivity (10·3 [8·7–12·2]) in contrast with residents of the lowest density quintile. County mobility restrictions that diminished place of job visits by now no longer lower than 5% in early March, 2020, had been connected to lower odds of seropositivity in July, 2020 (0·4 [0·3–0·5]) in contrast with a reduction of lower than 5%.

Interpretation

All around the major wave of the COVID-19 pandemic, fewer than 10% of the US grownup inhabitants fashioned antibodies against SARS-CoV-2, and fewer than 10% of those with antibodies had been diagnosed. Public health efforts to restrict SARS-CoV-2 spread devour to especially map racial and ethnic minority and densely populated communities.

Funding

Ascend Scientific Laboratories.

Introduction

Excessive acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus stimulates a immediate antibody response in people with symptomatic

  • Pollán M
  • Pérez-Gómez B
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  • et al.

Occurrence of SARS-CoV-2 in Spain (ENE-COVID): a nationwide, inhabitants-primarily based fully mostly seroepidemiological belief.

  • Hung IF
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  • et al.

SARS-CoV-2 shedding and seroconversion among passengers quarantined after disembarking a cruise ship: a case series.

  • Long QX
  • Liu BZ
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  • et al.

Antibody responses to SARS-CoV-2 in patients with COVID-19.

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  • Howard BM
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Scientific validity of serum antibodies to SARS-CoV-2: a case-assist watch over belief.

US Meals and Drug Administration

EUA approved serology test performance.

and asymptomatic

  • Hung IF
  • Cheng VC
  • Li X
  • et al.

SARS-CoV-2 shedding and seroconversion among passengers quarantined after disembarking a cruise ship: a case series.

  • Sakurai A
  • Sasaki T
  • Kato S
  • et al.

Pure historical past of asymptomatic SARS-CoV-2 infection.

  • Payne DC
  • Smith-Jeffcoat SE
  • Nowak G
  • et al.

SARS-CoV-2 infections and serologic responses from a sample of US navy provider individuals—USS Theodore Roosevelt, April 2020.

infection. Seroprevalence of SARS-CoV-2 antibodies in a inhabitants thus serves as an more cost effective measure of publicity and spread. Seroprevalence surveys in the United States, alternatively, had been restricted to single hotspots

  • Sood N
  • Simon P
  • Ebner P
  • et al.

Seroprevalence of SARS-CoV-2-particular antibodies among adults in Los Angeles County, California, on April 10–11, 2020.

  • Bendavid E
  • Mulaney B
  • Sood N
  • et al.

COVID-19 antibody seroprevalence in Santa Clara County, California.

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and prognosis of SARS-CoV-2 infection in Recent York.

or below-represented high-risk or vulnerable populations.

  • Bendavid E
  • Mulaney B
  • Sood N
  • et al.

COVID-19 antibody seroprevalence in Santa Clara County, California.

  • Havers F
  • Reed C
  • Lim T
  • et al.

Seroprevalence of antibodies to SARS-CoV-2 in six sites in the United States, March 23-Would possibly perhaps perchance well 3, 2020.

Furthermore, these reviews face challenges to successfully timed repetition and longitudinal apply-up, limiting their utility for surveillance.

  • Sood N
  • Simon P
  • Ebner P
  • et al.

Seroprevalence of SARS-CoV-2-particular antibodies among adults in Los Angeles County, California, on April 10–11, 2020.

  • Bendavid E
  • Mulaney B
  • Sood N
  • et al.

COVID-19 antibody seroprevalence in Santa Clara County, California.

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and prognosis of SARS-CoV-2 infection in Recent York.

Sufferers receiving dialysis will possible be belief about an supreme sentinel inhabitants wherein to belief the evolution of the COVID-19 public health crisis. Sufferers receiving dialysis in the United States undergo routine monthly laboratory reviews to gauge the effectiveness of therapy and to show mask mask for associated complications. In haemodialysis, usual get entry to to the bloodstream abrogates the need for phlebotomy to attain blood samples. Probability factors for acquisition of SARS-CoV-2 and for severe COVID-19, including evolved age, non-white elope, poverty, and diabetes, are the rule of thumb in preference to the exception in the US dialysis inhabitants.

United States Renal Data Machine

2018 annual records portray: epidemiology of kidney disease in the United States.

Learn in context

Evidence prior to this belief

Measuring the seroprevalence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibodies presents a entire review of its community spread. Community seroprevalence surveys require important infrastructure and expense, and face implementation challenges at some stage in the COVID-19 pandemic due to the restricted outreach in the worst-affected communities. Of the two biggest seroprevalence surveys in the United States, one was once restricted completely to Recent York affirm (n=15 101) and frail convenience sampling at grocery stores. A second glance frail remainder plasma from people visiting commercial laboratories in six cities (n=11 933), nonetheless lacked details on elope and ethnicity and assorted community-level risk factors.

Added value of this belief

We examined the leisure plasma of 28 503 patients receiving dialysis all the plan in which by technique of the United States, utilizing a chemiluminescence assay with high sensitivity and specificity. To our recordsdata, we present the major nationally handbook estimate of SARS-CoV-2 seroprevalence in the US dialysis and US grownup inhabitants, and estimates for differences in seroprevalence by neighbourhood elope and ethnicity, poverty, inhabitants density, and mobility restriction. We moreover evaluate which of the present measures of COVID-19 incidence most carefully correlate with seroprevalence. Most importantly, we reveal that as patients receiving dialysis devour monthly blood draws, with out fail and with out bias, and are a inhabitants with increased illustration of racial and ethnic minorities, repeated negative-sectional analyses of seroprevalence inner this sentinel inhabitants will also be performed as a challenging and honest surveillance approach in the United States.

Implications of the total obtainable proof

Same to records from assorted extremely affected nations and areas (eg, Spain and Wuhan, China), no topic the unparalleled stress on sources and unparalleled extra mortality being experienced in the United States at some stage in the COVID-19 pandemic, fewer than 10% of US adults had fashioned antibodies to SARS-CoV-2 as of July, 2020. There was once necessary regional variation from lower than 5% incidence in the west to extra than 25% in the northeast. Public health efforts to curb the spread of the virus devour to continue, with accept as true with one of the necessary most final discover-risk communities that we acknowledged, reminiscent of majority Shadowy and Hispanic neighbourhoods, poorer neighbourhoods, and densely populated metropolitan areas. A surveillance approach relying on monthly checking out of remainder plasma of patients receiving dialysis can invent honest estimates of SARS-CoV-2 spread inclusive of anxious-to-reach, deprived populations in the United States. Such surveillance can speak disease trends, resource allocation, and effectiveness of community interventions at some stage in the COVID-19 pandemic.

Discovering out remainder plasma from monthly samples got for routine care of patients on dialysis for SARS-CoV-2 antibodies therefore represents a challenging plan to a inhabitants-handbook surveillance approach,

  • Peeling RW
  • Wedderburn CJ
  • Garcia PJ
  • et al.

Serology checking out in the COVID-19 pandemic response.

informing dangers confronted by a vulnerable inhabitants while making creep illustration from racial and ethnic minorities. As well, seroprevalence surveys in patients receiving dialysis will also be linked to affected person-level and community-level records to enable evaluate and quantification of differences in SARS-CoV-2 incidence by demographic and neighbourhood strata, and thus facilitate effective mitigation suggestions focusing on the final discover-risk folks and communities.

In partnership with a commercial scientific laboratory, we examined seroprevalence of SARS-CoV-2 antibodies in a randomly chosen handbook sample of patients. Our aim was once to present a nationwide estimate of publicity to SARS-CoV-2 at some stage in the major wave of COVID-19 in the United States, up to July, 2020, with stratification by internet site, age, sex, and elope and ethnicity. We moreover harnessed inhabitants records on SARS-CoV-2 cases and deaths and percentage checking out definite utilizing nasal swab checking out to assess how seroprevalence estimates correlated with assorted epidemiological measures of COVID-19 incidence. Lastly, to speak preventive suggestions for the high-risk dialysis inhabitants as successfully as the usual inhabitants, we investigated community-level correlates for seropositivity.

Ideas

 Search for homicide and individuals

We did a negative-sectional prognosis of grownup (≥18 years) patients present process monthly laboratory checking out at Ascend Scientific utilizing samples got for routine scientific care that in any other case would had been discarded. Ascend Scientific is a commercial scientific laboratory primarily based fully mostly in Redwood Metropolis, California, that receives samples from a nationwide network of around 1300 dialysis amenities, serving approximately 65 000 patients. We randomly chosen patients from the affected person checklist on June 15, 2020, for seroprevalence checking out to be done in July, 2020, utilizing implicit stratification by internet site, age, sex, and elope and ethnicity followed by systematic sampling with fractional polynomials.

After sample selection and processing, Ascend Scientific sent anonymised records on affected person age, sex, elope and ethnicity, and build and facility ZIP codes to Stanford University investigators for analyses. Stanford University investigators extra linked affected person geographical recordsdata (ZIP code) to census records and publicly obtainable COVID-19 burden and community mobility records. The belief bought expedited approval from the Stanford University of Medicine Institutional Overview Board; urged consent was once waived.

 Procedures

We frail the US Meals and Drug Administration-approved Siemens Healthineers SARS-CoV-2 spike protein receptor binding domain (S1RBD) complete antibody (immunoglobulin) chemiluminescence assay, which has 100% sensitivity (≥14 days after a definite PCR test) and 99·8% specificity.

US Meals and Drug Administration

EUA approved serology test performance.

We selected this assay on the basis of its Emergency Exhaust Authorization in June, 2020, in the context that S1RBD is moreover the map of vaccine construction efforts.

US Meals & Drug Administration

Search for of antibody response to SARS-CoV-2 spike proteins would possibly again speak vaccine homicide.

Sample processing is detailed in the appendix (p 3)).

We linked affected person-level build records with cumulative and on every day basis cases and deaths per 100 000 inhabitants as compiled on a county level by the Heart for Methods Science and Engineering at Johns Hopkins University

  • Dong E
  • Du H
  • Gardner L

An interactive internet-primarily based fully mostly dashboard to trace COVID-19 in steady time.

and with nasal swab test positivity rates, as compiled on a affirm level by the Covid Tracking Project.

The COVID Tracking Project

Data API.

For Utah, we followed the Utah Department of Neatly being groupings of several smaller counties and extracted records true now.

Utah Department of Neatly being

Overview of COVID-19 surveillance.

Recent York Metropolis records are now no longer obtainable by county all the plan in which by technique of the Johns Hopkins University dataset; therefore, we true now extracted records from the Recent York Metropolis Dashboard.

NYC Neatly being

COVID-19: records, by borough.

For county-level mobility restrictions, we frail Google Mobility Data that portray a median percentage change in the series of place of job visits over the length March 1–15, 2020, prior to the implementation of refuge-in-internet site restrictions in the massive majority of the country. Percentage modifications in the Google Mobility records are listed to a corresponding weekday (eg, Tuesdays are matched to Tuesdays) from Jan 3 to Feb 6, 2020.

Google

Google COVID-19 community mobility reviews.

We moreover linked affected person-level build records with ZIP code tabulation build (ZCTA) records from the 2018 American Community Gawk (ACS) 5-year estimates

US Census Bureau American Community Gawk

2018 American Community Gawk 5 year estimates, tables B03002, S1701, and B01003.

to examine affected person neighbourhood percentage dwelling under the poverty level and elope and ethnicity mix, and with American Census Bureau 2010 estimates

US Census Bureau

Zip code tabulation areas (ZCTA).

to examine inhabitants density. We outlined ZCTA majority elope and ethnicity as Hispanic, non-Hispanic Shadowy, or non-Hispanic white if the inhabitants in the ZCTA was once now no longer lower than 60% Hispanic, non-Hispanic Shadowy, or non-Hispanic white, respectively; the build this was once now no longer the case, if the Hispanic and Shadowy inhabitants mixed was once now no longer lower than 60% of the inhabitants, the ZCTA majority was once outlined as Hispanic and Shadowy, in any other case as assorted. For city versus rural ZCTA internet site, we frail the 2010 Rural Urban Commuting Build codes by census tract, categorising a ZCTA as dense city, metropolitan, micropolitan, or minute city or rural build if extra than 50% of the inhabitants in the ZCTA was once dwelling in a single of these build codes.

United States Department of Agriculture

2010 rural-city commuting build (RUCA) codes.

 Statistical prognosis

We assumed a nationwide incidence of SARS-CoV-2 antibody of 5%.

  • Sood N
  • Simon P
  • Ebner P
  • et al.

Seroprevalence of SARS-CoV-2-particular antibodies among adults in Los Angeles County, California, on April 10–11, 2020.

  • Benatia D
  • Godefroy R
  • Lewis J

Estimating COVID-19 incidence in the United States: a sample selection mannequin plan.

To generate incidence estimates for patients on dialysis utilizing preselected regional strata with precision inner 0·5%, a sample of 27 364 was once required (appendix p 2). In accordance with old trends, we expected 15% of chosen samples to be unavailable in July, 2020, due to the loss of life, switch to assorted amenities, or assorted reasons for missing laboratory records (eg, hospitalisation or non-adherence). Accounting for this capability dropout, we randomly chosen 31 509 patients.

We present incidence estimates with 95% CIs in our sample, standardised to the US grownup dialysis inhabitants and to the US grownup inhabitants. For the US grownup dialysis inhabitants, we frail the distribution of all adults receiving repairs dialysis, as adverse to those dwelling in the territories, on Jan 1, 2017, acknowledged by technique of the United States Renal Data Machine database. For the US grownup inhabitants, we frail 2018 ACS 1-year estimates.

US Census Bureau American Community Gawk

2018 American Community Gawk 5 year estimates, tables B03002, S1701, and B01003.

In accordance with the test sensitivity range got by Schnurra and colleagues of their exterior validation,

  • Schnurra C
  • Reiners N
  • Biemann R
  • Kaiser T
  • Trawinski H
  • Jassoy C

Comparability of the diagnostic sensitivity of SARS-CoV-2 nucleoprotein and glycoprotein-primarily based fully mostly antibody tests.

we moreover present test characteristic-adjusted sample inhabitants estimates, ranging sensitivity from 85% to 98%.

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and prognosis of SARS-CoV-2 infection in Recent York.

To compute the percentage of estimated seroprevalent cases that had been at risk of be diagnosed cases,

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and prognosis of SARS-CoV-2 infection in Recent York.

  • Stringhini S
  • Wisniak A
  • Piumatti G
  • et al.

Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a inhabitants-primarily based fully mostly belief.

we in contrast the estimated seroprevalent cases per 100 000 grownup inhabitants with Johns Hopkins University estimates of cumulative diagnosed cases per 100 000 US grownup inhabitants as of June 15, 2020.

To standardise estimates, we assigned weights to every particular person per their membership to every of 32 strata of census areas (northeast, south, midwest, and west), age (18–44, 45–64, 65–79, and ≥80 years), and sex. We outlined put up-stratification weights as the percentage of every stratum represented in the US dialysis inhabitants or US grownup inhabitants divided by the analogous percentage in the sample.

  • Kolenikov S

Publish-stratification or non-response adjustment?.

  • Korn EL
  • Graubard BI

Prognosis of health surveys.

We then computed weighted frequencies and 95% CIs per four prespecified strata (internet site, age, sex, and elope and ethnicity) with differences evaluated utilizing Rao-Scott χ2 tests.

  • Rao JNK
  • Scott AJ

The prognosis of categorical records from complex surveys: chi-squared tests for goodness of match and independence in two-manner tables.

  • Rao JNK
  • Scott AJ

On chi-squared tests for multiway contingency tables with cell properties estimated from glance records.

Attributable to the missingness of elope and ethnicity records in the electronic health records, we frail the additional measure of ZCTA elope and ethnicity distribution with categories tailored from Moore and colleages.

  • Moore LV
  • Diez Roux AV
  • Evenson KR
  • McGinn AP
  • Brines SJ

Availability of leisure sources in minority and low socioeconomic internet site areas.

  • Bower KM
  • Thorpe Jr, RJ
  • Rohde C
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The intersection of neighborhood racial segregation, poverty, and urbanicity and its impact on food retailer availability in the United States.

Next, we correlated five measures of COVID-19 incidence—cumulative cases on June 15, 2020 (or first obtainable date between June 15 and June 30, 2020); cumulative deaths on June 30, 2020 (or last obtainable date between June 15 and June 30, 2020); 15-day averages of on every day basis cases and on every day basis deaths; and percentage checking out definite on nasal swab tests between June 15 and June 30, 2020—with SARS-CoV-2 seroprevalence in patients on dialysis in July, 2020. To enact this, we first collapsed all measures to a affirm level after which assessed the Spearman’s correlation coefficient ρ for the affiliation of every measure with seroprevalence. Thanks to the high density of Ascend Scientific amenities in Recent York, Texas, and California, we moreover selected those states to present county-level correlations.

Lastly, utilizing logistic regression, we creep the age-adjusted and sex-adjusted correlates of seropositivity for affected person ZCTA elope and ethnicity distribution, percentage dwelling under poverty level, rural or city classification, inhabitants density, and county mobility restriction.

We assumed statistical significance at α<0·05. All statistical analyses were done with SAS Enterprise Guide (version 7.1) and Stata (version 15.1).

 Role of the funding source

Ascend Clinical Laboratories supported the remainder plasma testing for SARS-CoV-2 antibodies. SA, MM-R, and JH had complete access to all data in the study and SA, MM-R, JH, JP, and GMC were responsible for the decision to submit for publication.

Results

Of the 31 509 people selected for testing on June 15, 2020, 28 503 were tested in July, 2020 (figure 1), with 25 217 (88·5%) tested in the first 2 weeks (appendix p 4). The sampling was representative of the US dialysis patient distribution by age, sex, race and ethnicity (when excluding patients without race and ethnicity data), and region, except sampled patients were less likely to be non-Hispanic Black (table 1). Compared with the US adult population, our sampled patient population was older, had more men, and was more likely to be non-Hispanic Black and living in non-white neighbourhoods (table 1). A greater proportion of our sampled population and the US dialysis population lived in the west, and a lower proportion lived in the midwest, compared with the US adult population. Patients in our sample lived in 46 states and in 1013 (32%) of 3141 US counties (appendix p 6).

Figure thumbnail gr1

Table 1Comparison of sampled population, US adult dialysis population, and US adult population

US adult population given is for 2018 and US adult patients dialysis population as of Jan 1, 2017. ZCTA=ZIP code tabulation area.

Overall, sample seroprevalence was 8·0% (95% CI 7·7–8·4). Accounting for the externally validated test sensitivity,

  • Schnurra C
  • Reiners N
  • Biemann R
  • Kaiser T
  • Trawinski H
  • Jassoy C

Comparison of the diagnostic sensitivity of SARS-CoV-2 nucleoprotein and glycoprotein-based antibody tests.

seroprevalence ranged from 8·2% (7·9–8·5) to 9·4% (9·1–9·8) in our sampled population (appendix p 7). When standardised to the US dialysis population, seroprevalence was 8·3% (8·0–8·6), with high regional variation in seroprevalence (ranging from 3·5% [3·1–3·9] in the west to 27·2% [25·9–28·5] in the northeast; table 2). Seroprevalence was similar by sex and modestly lower in people aged 80 years or older compared with those aged 45–64 years (table 2). Differences in seroprevalence by race and ethnicity were similar using both our patient-level (electronic health record) and neighbourhood-level (ZCTA majority race and ethnicity) measures, with non-Hispanic Black patients having the highest seropositivity, followed by Hispanic patients, and non-Hispanic white patients having the lowest.

Table 2Seroprevalence of SARS-CoV-2 antibodies in patients receiving dialysis in the USA

SARS-CoV-2=severe acute respiratory syndrome coronavirus 2. ZCTA=ZIP code tabulation area.

We estimated the SARS-CoV-2 standardised seroprevalence in the US population to be 9·3% (95% CI 8·8–9·9; table 3). Based on the Johns Hopkins University cumulative case data as of June 15, 2020, the prevalence of (nasal swab) diagnosed cases was 826 per 100 000 US adult population, compared with our estimate of 8989 seropositive people per 100 000 population, meaning that 9·2% (8·7–9·8) of seropositive people were diagnosed.

Using data from our sampled population, variation by state was high, ranging from 0·0% in seven states to 33·6% (31·7–35·6) in New York, with the highest regional variation occurring in the northeast (figure 2; appendix pp 8–9). When comparing state seroprevalence against cumulative cases and deaths per 100 000 population, deaths correlated best (ρ=0·66 for cases vs 0·77 for deaths; figure 3). The percentage of people testing positive by nasal swab test and 15-day average of daily deaths in the latter half of June, 2020, showed a weaker correlation (ρ=0·58 and 0·66, respectively), whereas 15-day average of daily cases did not correlate with seroprevalence (ρ=−0·14). On a county level in California, New York, and Texas, there was even more heterogeneity in the correlation between seroprevalence and other disease measures (ρ≤0·51 for all correlations for all three states’ county-level data; appendix p 10).

Figure thumbnail gr3

Figure 3Cumulative cases (A) and cumulative deaths (B) per 100 000 population, by state

Data are in the US population as of June 15 (A) and June 30 (B), 2020.

  • Dong E
  • Du H
  • Gardner L

An interactive web-based dashboard to track COVID-19 in real time.

Utah Department of Health

Overview of COVID-19 surveillance.

NYC Health

COVID-19: data, by borough.

US Census Bureau American Community Survey

2018 American Community Survey 5 year estimates, tables B03002, S1701, and B01003.

States in white were not included in the sample.

Likelihood of SARS-CoV-2 seropositivity was lower among older people (odds ratio 0·8 [95% CI 0·7–0·9] for people aged 80 years or older vs people aged 45–64 years), but did not differ by sex (1·0 [0·9–1·1] for women vs men). In age-adjusted and sex-adjusted models, neighbourhood racial and ethnic distribution, poverty level, dense urbanisation, population density, and percentage change in workplace visits in early March, 2020, were all strongly associated with seropositivity (figure 4).

Figure thumbnail gr4

Figure 4Forest plot for odds of SARS-CoV-2 seropositivity

All variables are at a neighbourhood (ie, ZCTA) level, except for reduction in workplace visits, which is at a county level, and are modelled separately, accounting for age and sex. Poverty level is defined as percentage of people living below the federal poverty level in the ZCTA. Population density quintiles are derived from the ZCTA (median 2884 people per square mile [IQR 603–6800]). Reductions in workplace visits were measured during the first 2 weeks of March, 2020, compared with a baseline in January–February, 2020. OR=odds ratio. SARS-CoV-2=severe acute respiratory syndrome coronavirus 2. ZCTA=ZIP code tabulation area.

Discussion

In our analysis of seroprevalence of SARS-CoV-2 spike protein receptor binding antibodies from a nationwide representative sample of patients receiving dialysis, we find that despite the USA contemporaneously leading the world in the numbers of diagnosed cases, overall, fewer than 10% of US adults had evidence of seroconversion in July, 2020. A vast majority of US adults, including people receiving dialysis who are among the highest risk for mortality upon contracting SARS-CoV-2,

  • Alberici F
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  • Manenti C
  • et al.

A report from the Brescia Renal COVID Task Force on the clinical characteristics and short-term outcome of hemodialysis patients with SARS-CoV-2 infection.

do not have evidence of exposure or immune response. Furthermore, we find increased likelihood of SARS-CoV-2 seropositivity in residents of predominantly Black and Hispanic neighbourhoods (two to three times higher), poorer areas (two times higher), and the most densely populated areas (ten times higher). Early reduction in community mobility in March, 2020, was associated with 60% lower likelihood of individual-level seroconversion by July that year.

Unlike most published estimates of SARS-CoV-2 seroprevalence from the USA,

  • Sood N
  • Simon P
  • Ebner P
  • et al.

Seroprevalence of SARS-CoV-2-specific antibodies among adults in Los Angeles County, California, on April 10–11, 2020.

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York.

  • Havers F
  • Reed C
  • Lim T
  • et al.

Seroprevalence of antibodies to SARS-CoV-2 in six sites in the United States, March 23-May 3, 2020.

patients included in our study sample had antibodies measured from blood collected as part of routine medical care. Thus, our prevalence estimates should not be subject to selection bias due to presence versus absence of symptoms, availability of testing materials, local or regional testing strategies, geography, income, educational attainment, language proficiency, immigration status, mobility, anxiety, fear, or other factors. Moreover, since end-stage kidney disease qualifies affected patients for Medicare insurance, and since end-stage kidney disease disproportionately affects Black, Hispanic, and other disadvantaged populations,

United States Renal Data System

2018 annual data report: epidemiology of kidney disease in the United States.

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  • et al.

Neighborhood poverty and racial differences in ESRD incidence.

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  • et al.

Low income, community poverty and risk of end stage renal disease.

we are able to determine—with a high level of precision—differences in seroprevalence among patient groups within and across regions of the USA. Of the two larger seroprevalence surveys published from the USA thus far, one was confined to New York state (n=15 101), employed a convenience sampling technique at grocery stores, and relied on a microsphere immunoassay with lower sensitivity.

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York.

The second, the Centers for Disease Control and Prevention (CDC) Six Sites study (n=11 933), used remainder plasma from people getting testing for undefined clinical indications, and did not have detailed sociodemographic information about the tested people.

  • Havers F
  • Reed C
  • Lim T
  • et al.

Seroprevalence of antibodies to SARS-CoV-2 in six sites in the United States, March 23-May 3, 2020.

Uncertainty exists as to whether seroprevalence estimates in the dialysis population can be extrapolated to the US population more broadly. A recent analysis of SARS-CoV-2 IgG antibodies in two dialysis units in London, UK, reported seroprevalence of 36%, higher than in healthy blood donors (15%) but lower than in health-care workers (45%) sampled within a similar time frame.

  • Clarke C
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  • et al.

High prevalence of asymptomatic COVID-19 infection in hemodialysis patients detected using serologic screening.

Our data might overestimate overall seroprevalence in the general population since patients on dialysis are disproportionately from racial and ethnic minorities;

  • Choi AI
  • Rodriguez RA
  • Bacchetti P
  • Bertenthal D
  • Hernandez GT
  • O’Hare AM

White/black racial differences in risk of end-stage renal disease and death.

  • Hsu CY
  • Lin F
  • Vittinghoff E
  • Shlipak MG

Racial differences in the progression from chronic renal insufficiency to end-stage renal disease in the United States.

for example, Black Americans have a nearly four-times higher risk of end-stage kidney disease than white Americans.

United States Renal Data System

2018 annual data report: epidemiology of kidney disease in the United States.

Moreover, the process of undergoing in-centre haemodialysis might include the use of public or non-public shared transportation to and from the facility, and 10–12 h of care delivered in indoor facilities.

Conversely, these data might underestimate overall seroprevalence in the general population. Patients receiving dialysis are less likely to be employed

  • Erickson KF
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  • Winkelmayer WC

Employment among patients starting dialysis in the United States.

and more likely to restrict their mobility and social activity due to advanced age and frailty;

  • Bao Y
  • Dalrymple L
  • Chertow GM
  • Kaysen GA
  • Johansen KL

Frailty, dialysis initiation, and mortality in end-stage renal disease.

therefore, they might have fewer opportunities to acquire the infection, particularly from asymptomatic individuals. Extrapolating from multiple prospective hepatitis B immunisation studies—in which 50–75% of vaccinated patients receiving dialysis mounted a response compared with 95% or more people from the general population—patients receiving dialysis might mount a weaker immune response and thus be less likely to seroconvert.

  • Edey M
  • Barraclough K
  • Johnson DW

Review article: hepatitis B and dialysis.

Finally, patients receiving dialysis might have been more likely to die or have been hospitalised due to complications of SARS-CoV-2 infection. If so, these patients would not have been present for testing in the dialysis facilities, creating a survival bias and yielding lower estimates of exposure.

Nonetheless, the ten-times difference we observed between diagnosed cases per 100 000 population and our estimates of seropositive people per 100 000 has been similarly reported in studies from New York,

  • Rosenberg ES
  • Tesoriero JM
  • Rosenthal EM
  • et al.

Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York.

the CDC Six Sites study,

  • Havers F
  • Reed C
  • Lim T
  • et al.

Seroprevalence of antibodies to SARS-CoV-2 in six sites in the United States, March 23-May 3, 2020.

and in a population-representative analysis from Geneva.

  • Stringhini S
  • Wisniak A
  • Piumatti G
  • et al.

Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study.

Thus, our findings comport with other seroprevalence estimates. We confirm that as in other studies from COVID-19 hotspots,

  • Pollán M
  • Pérez-Gómez B
  • Pastor-Barriuso R
  • et al.

Prevalence of SARS-CoV-2 in Spain (ENE-COVID): a nationwide, population-based seroepidemiological study.

  • Stringhini S
  • Wisniak A
  • Piumatti G
  • et al.

Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study.

  • Xu X
  • Sun J
  • Nie S
  • et al.

Seroprevalence of immunoglobulin M and G antibodies against SARS-CoV-2 in China.

a minority of the population has evidence of exposure and immune response, and a vast majority, including people at high risk for mortality (ie, the population on dialysis), remain vulnerable. In fact, even if the seroprevalence estimates derived from the US dialysis population overestimated true seroprevalence in the overall US adult population, our data nonetheless support that fewer than 10% of the US population has seroconverted as of July, 2020, and herd immunity remains out of reach, as has been the conclusion from large international surveys from the UK

  • Ward HAC
  • Whitaker M
  • et al.

Antibody prevalence for SARS-CoV-2 in England following first peak of the pandemic: REACT2 study in 100,000 adults.

and Spain,

  • Pollán M
  • Pérez-Gómez B
  • Pastor-Barriuso R
  • et al.

Prevalence of SARS-CoV-2 in Spain (ENE-COVID): a nationwide, population-based seroepidemiological study.

where intense outbreaks of COVID-19 occurred during the spring and summer of 2020.

Furthermore, the seroprevalence differences captured by region, age, sex, and community-level risk factors (ie, internal comparisons) are expected to be similar in the US dialysis and US general adult population. Our study provides convincing evidence that the COVID-19 pandemic has dramatically amplified existing health disparities. Data from the CDC highlighting SARS-CoV-2 health disparities evaluate hospitalisations and deaths by race and ethnicity,

Centers for Disease Control and Prevention

COVIDView: a weekly surveillance summary of US Covid-19 activity.

  • Cowger TL
  • Davis BA
  • Etkins OS
  • et al.

Comparison of weighted and unweighted population data to assess inequities in coronavirus disease 2019 deaths by race/ethnicity reported by the US Centers for Disease Control and Prevention.

calling into question whether Black and Hispanic populations are experiencing more severe illness versus facing higher likelihoods of exposure. Some US state dashboards also report higher cumulative cases among Black and Hispanic people compared with non-Hispanic white people,

  • Yancy CW

COVID-19 and African Americans.

but none have as precisely quantified differences on a national level.

Neighbourhood poverty and population density were also highly correlated with seroprevalence, with a possible threshold effect for population density, such that there was a ten-times higher risk in the highest density ZCTAs (>8607 people per sq. mile). Inhabitants density is recognised as a a must-devour command, utilizing the spread in metropolitan areas, in confined spaces (eg, the Diamond Princess cruise ship), tremendous gatherings (eg, the Recent Orleans’ Mardi Gras),

  • Bialek S
  • Bowen V
  • Chow N
  • et al.

Geographic differences in COVID-19 cases, deaths, and incidence—United States, February 12-April 7, 2020.

  • Sy KTL
  • White LF
  • Nichols BE

Inhabitants density and traditional reproductive series of COVID-19 across United States counties.

and in populous areas across the arena.

  • Baqui P
  • Bica I
  • Marra V
  • Ercole A
  • van der Schaar M

Ethnic and regional adaptations in sanatorium mortality from COVID-19 in Brazil: a negative-sectional observational belief.

Rocklöv and Sjödin counsel that the elemental reproduction quantity (R0) of SARS-CoV-2 will improve linearly with inhabitants density.

  • Rocklöv J
  • Sjödin H

High inhabitants densities catalyse the spread of COVID-19.

Our records moreover reveal a minute bit lower likelihood of seropositivity among older people, as was once considered in a present portray from Geneva

  • Stringhini S
  • Wisniak A
  • Piumatti G
  • et al.

Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a inhabitants-primarily based fully mostly belief.

and attributed to higher adherence to bodily distancing measures by the authors. A bigger competing risk from hospitalisations or mortality after SARS-CoV-2 publicity will possible be a increased contributing command in the seen lower seroprevalence in older in contrast with younger age groups.

As well to offering an total estimate of SARS-CoV-2 seroprevalence and quantifying differences by affected person and community characteristics, our belief locations forth a viable surveillance approach for SARS-CoV-2 spread in the United States. WHO and assorted consultants

  • Peeling RW
  • Wedderburn CJ
  • Garcia PJ
  • et al.

Serology checking out in the COVID-19 pandemic response.

  • Koopmans M
  • Haagmans B

Assessing the extent of SARS-CoV-2 circulation by technique of serological reviews.

advocate for repeated negative-sectional analyses of seroprevalence as a disease monitoring device in a self-discipline to most fully measure the gorgeous incidence of SARS-CoV-2, since these can extra possible consume incidence of publicity in every symptomatic and asymptomatic folks. Undoubtedly, we seen enormous heterogeneity in the correlation between seroprevalence and assorted measures of SARS-CoV-2 that are presently being frail—as adverse to deaths per 100 000, that are a gradual

  • Grasselli G
  • Greco M
  • Zanella A
  • et al.

Probability factors connected to mortality among patients with COVID-19 in intensive care devices in Lombardy, Italy.

—supporting the utilization of posthaste instituted seroprevalence surveys as a complementary surveillance tool. Extra public health implications of seroprevalence surveys encompass assessing checking out adequacy. As an illustration, in states the build the variation between seropositive and diagnosed cases is reducing over time, checking out skill is at risk of be rising. Furthermore, following seroconversion rates over time can presage hospitalisations and intensive care unit stays, for the explanation that point between publicity and seroconversion is comparatively immediate (median 10 days),

  • Stringhini S
  • Wisniak A
  • Piumatti G
  • et al.

Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a inhabitants-primarily based fully mostly belief.

and would possibly therefore facilitate resource allocation. Lastly, as we reveal by assessing community mobility restrictions, seroprevalence surveys can measure the outcomes of interventions to treat or prevent infection with SARS-CoV-2.

  • Peeling RW
  • Wedderburn CJ
  • Garcia PJ
  • et al.

Serology checking out in the COVID-19 pandemic response.

Repeated serological surveys, if done in a community environment, would require intensive sources and yet stay self-discipline to selection bias. On the opposite hand routine monthly checking out of remainder plasma of randomly chosen sets of people—as is practically possible in patients receiving dialysis—can assist as a handbook surveillance device in the United States, with minimal phlebotomy or infrastructure requirement, and as our records reveal, encompass traditionally below-represented and socially deprived groups.

This prognosis has an incredible series of strengths. We frail a extremely particular and sensitive immunoassay, one which has been robustly linked to SARS-CoV-2 publicity.

  • Peeling RW
  • Wedderburn CJ
  • Garcia PJ
  • et al.

Serology checking out in the COVID-19 pandemic response.

  • Schnurra C
  • Reiners N
  • Biemann R
  • Kaiser T
  • Trawinski H
  • Jassoy C

Comparability of the diagnostic sensitivity of SARS-CoV-2 nucleoprotein and glycoprotein-primarily based fully mostly antibody tests.

  • Liu W
  • Liu L
  • Kou G
  • et al.

Evaluate of nucleocapsid and spike protein-primarily based fully mostly enzyme-linked immunosorbent assays for detecting antibodies against SARS-CoV-2.

Public Neatly being England

Evaluate of sensitivity and specificity of 4 commercially obtainable SARS-CoV-2 antibody immunoassays.

The belief sample was once extremely handbook of the US dialysis inhabitants and, as successfully-known, we frail remainder plasma from specimens frail in routine scientific care. The sample size and sampling device allowed us to estimate with precision incidence across several affected person characteristics. Furthermore, linking to US Census and assorted publicly obtainable records sources assembled at some stage in the pandemic presents treasured context when brooding in regards to the implications of these records to the usual inhabitants. There are moreover several crucial boundaries. As successfully-known beforehand, it’s plausible that seroprevalence estimates from the US dialysis inhabitants overestimate seroprevalence in the US grownup inhabitants. We enact now no longer devour affected person-level records on indicators nor nasal swab checking out outcomes, and thus can not test whether or now no longer the likelihood of seroconversion differs in patients receiving dialysis from on the total wholesome adults, even though preliminary records from London, UK, counsel no differences.

  • Clarke C
  • Prendecki M
  • Dhutia A
  • et al.

High incidence of asymptomatic COVID-19 infection in hemodialysis patients detected utilizing serologic screening.

We moreover enact now no longer devour affected person-level records on health internet site, employment internet site, profits, household size, dwelling house, and assorted sociodemographic factors, and so relied on neighbourhood proxies for plenty of these domains. Dialysis devices are extra in general situated in city areas, and thus we now devour below-illustration of rural areas. Lastly, while tremendous, our belief was once designed for steady regional, now no longer affirm-level or county-level, estimates.

In conclusion, we present SARS-CoV-2 seroprevalence records in a broadly handbook sample of patients receiving dialysis across the United States and reveal striking differences in seroprevalence by several affected person characteristics, with bigger seroprevalence in younger patients, Shadowy and Hispanic patients, and patients dwelling in poorer and majority-minority neighbourhoods. These records can again to speak surveillance and administration suggestions at some stage in the next a part of the pandemic. Serial sampling of dialysis remainder plasma must aloof be frail to uncover trends in disease incidence and the produce of assorted suggestions being performed around the United States to lower the burden of COVID-19 on the usual inhabitants.

Contributors

SA assisted with records cleansing and prognosis planning, and manuscript writing. MM-R developed the prognosis notion, generated census records tables, supervised records prognosis, and contributed to manuscript writing. JH undertook records cleansing and prognosis, including linkage to exterior records and figure generation, and contributed to manuscript writing. JB undertook sample processing and records preparation and contributed to manuscript writing. RK chosen seroprevalence checking out, supervised sample processing, and contributed to manuscript writing. PB co-conceived the belief, secured seroprevalence checking out, and supervised sample processing and records preparation. JP supervised the belief prognosis notion, acknowledged relevant exterior records, contributed to records interpretation, and supervised manuscript writing. GMC co-conceived the belief, supervised the belief prognosis notion, and co-wrote the manuscript.

Declaration of interests

JB, RK and PB are employed by Ascend Scientific Laboratories. GMC is on the Board of Administrators of Satellite tv for computer Healthcare, a now no longer-for-income dialysis organisation. All remaining authors speak no competing interests.

Data sharing

De-acknowledged negative-sectional records from the prognosis will also be made obtainable after authors’ evaluate of request of and would possibly require compilation of particular categories (eg, at the older age groups) to give protection to affected person privateness.

Acknowledgments

Ascend Scientific Laboratories supported the leisure plasma checking out for SARS-CoV-2 antibodies. SA was once supported by 5K23DK101826. MM-R and GC are supported by Nationwide Institutes of Neatly being NIDDK Ok24 DK085446 . We thank Martin Gorfinkel (Mountain Gaze, CA, USA) for his feedback on sampling homicide.

Supplementary Self-discipline topic

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Article Data

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Printed: September 25, 2020

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DOI: https://doi.org/10.1016/S0140-6736(20)32009-2

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© 2020 Elsevier Ltd. All rights reserved.

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