Inequality Fueled COVID-19 Transmission in San Francisco’s Mission District, Says New Study

Test Results Show Economic Factors Drove Increased Transmission in Latinx Essential Workers and Families Despite Shelter-in-Place

By Nicholas Weiler

nurse administers a nasal swab for COVID-19 testing at a Mission District testing site

Katie Machado, RN, UCSF Nurse Practitioner Student, conducts COVID-19 testing that was conducted by Unidos En Salud, a unique partnership between Mission community organizers in the Latino Task Force for COVID-19, UCSF researchers, the City and County of San Francisco, and the San Francisco Department of Public Health (DPH). Photo by Barbara Ries

In the first six weeks of San Francisco’s shelter-in-place ordinance, continued spread of COVID-19 was increasingly concentrated among low-income Latinx people who were unable to work from home, according to results of a community-based screening initiative conducted in San Francisco’s Mission District in late April.

A report of the results, from both nasal swab (PCR) and serological (antibody) tests, has been submitted to a peer-reviewed journal, and was also posted publicly on the medRxiv preprint server on June 17, 2020, due to the results’ importance for public health policy and affected communities.

The testing initiative, called Unidos En Salud, was spearheaded by UC San Francisco infectious disease experts and community organizers from the Latino Task Force for COVID-19. Along with recent initiatives to provide testing in the town of Bolinas and for housed and unhoused people in the Bayview, Sunnydale and Visitacion Valley neighborhoods in southeast San Francisco, the collaboration is part of UCSF’s tightly coordinated work with the San Francisco Department of Public Health, the state of California, and affected communities to respond to the public health crisis presented by COVID-19.

In partnership with the City and County of San Francisco, Unidos En Salud offered free PCR and antibody testing, regardless of symptoms, to all residents and workers in US census tract 229.01, a densely populated 16-square-block section of the Mission District, which has a large Latinx population. Including initial walk-up testing conducted April 25–28, and additional testing of home-bound residents in early May, the initiative ultimately reached 3,953 individuals.

“We find that recent infections in late April were concentrated almost exclusively among low-income Latinx people working frontline jobs, whereas infections earlier in the pandemic affected people more equally across the ethnic and economic spectrum,” said study principal investigator and senior author Diane Havlir, MD, chief of the UCSF Division of HIV, Infectious Diseases and Global Medicine at Zuckerberg San Francisco General Hospital and Trauma Center (ZSFG). “This suggests health effects of ethnic and socioeconomic inequities in the community increased during San Francisco’s shelter-in-place ordnance and helps explain why Latinx people have been disproportionately affected by the pandemic.”

Diane Havlir in SF's Mission District

Diane Havlir, MD, chief of the UCSF Division of HIV, Infectious Diseases and Global Medicine at Zuckerberg San Francisco General Hospital and Trauma Center

PCR tests found that 2.1 percent of participants were actively infected with the SARS-CoV-2 virus at the time of testing in late April, in line with preliminary results reported in May. Infection rates were nearly 20-fold higher in Latinx than non-Latinx participants (3.9 percent vs. 0.2 percent), and 3.5 times higher for non-resident workers than for residents of the census tract (6 percent vs. 1.7 percent).

Additionally, 3.1 percent of census tract residents and 7.7 percent of census tract workers tested positive for antibodies against the SARS-CoV-2 virus.

Adjusting for the known accuracy of PCR and antibody tests and for rates of participation in the testing initiative, the study team estimates that approximately 6.1 percent of all census tract residents were either actively infected or had been previously infected with the virus by the end of April. This figure is lower than estimates based on antibody testing alone in hard-hit areas like New York City, where 14.9 percent of the population was thought to have been infected by late April, and slightly higher than a recent antibody prevalence estimate of 4.65 percent for Los Angeles County residents in early April.

Comparison of PCR and antibody results for census tract residents revealed that, the vast majority (96 percent) of new infections were occurring in the Latinx community by the end of April, whereas those infected earlier in the pandemic were somewhat more representative of the neighborhood as a whole (67 percent Latinx, 16 percent white, 17 percent other). Other risk factors for recent infections in late April were inability to shelter in place and maintain income, frontline service work, unemployment, and household income of less than $50,000 per year.

“Although San Francisco’s early shelter-in-place order surely prevented the overwhelming numbers of hospitalizations and deaths that were seen in other parts of the country, the disproportionate effects on communities of color are similar to those we see elsewhere,” said Jon Jacobo, a leader of the Latino Task Force for Covid-19 and a co-author on the new preprint study.

High Levels of Virus in Persons With, Without Symptoms

The study also addressed the pressing question of how many people who test positive for SARS-CoV-2 infection experience symptoms. At the time of testing in late April, more than half of actively infected individuals (52 percent) had reported being asymptomatic. Of these individuals, 24 percent developed symptoms within two weeks after testing. Notably, the researchers found that recently infected individuals (those with positive nasal swab tests but negative antibody tests) showed high levels of viral infection regardless of whether they experienced symptoms, suggesting that they might continue to be infectious.

“These results emphasize the importance of community-based testing of both symptomatic and asymptomatic individuals to understand the spread of the virus,” said Gabriel Chamie, MD, MPH, an associate professor in the Division of HIV, Infectious Diseases and Global Medicine and lead author on the preprint study. “Symptom-based testing would have failed to detect over 40 percent of active infections, and only one person who tested positive required hospitalization, suggesting the vast majority – many of whom had high levels of virus – would not have been diagnosed without community-based testing.”

“A strong partnership with the Latino Task Force for COVID-19 was essential to providing low-barrier universal testing in the Mission to better understand the virus’s continued spread and to bring needed care and support for those who have been affected,” added Carina Marquez, MD, an assistant professor in the Division of HIV, Infectious Diseases, and Global Medicine who shares lead-authorship of the preprint study with Chamie.

Economic Hardship a Key Driver of Increased Transmission

The study also demonstrated the utility of analyzing the genomic sequences of the SARS-CoV-2 virus detected in the community through a collaboration with the Chan Zuckerberg Biohub. At least five different strains were detected, all of which had also been observed elsewhere in the city. “This is consistent with multiple independent introductions over time from people either living or working within the census tract, with subsequent transmission to family members sharing close living quarters,” said CZ Biohub Co-President Joe DeRisi, PhD, a professor of biochemistry and biophysics at UCSF and co-author on the new study.

These data further highlight the importance of economic factors, such as financial insecurity and skyrocketing rental costs in the city, in driving high rates of COVID-19 transmission, for which the Latinx community has been wrongly stigmatized, the study authors said.

“Pandemics exploit the existing inequities in society, putting a larger health and economic burden on communities who already face structural disadvantages such as income inequality, crowded housing conditions, systemic racism and discrimination,” said Grant Colfax, MD, San Francisco Director of Health. “Through our collaboration with UCSF, we can document the social and economic factors that put people more at risk of getting COVID-19. San Francisco’s Latinx population is over-represented among positive COVID-19 cases, and studies like this one help us to understand why and inform action and further community partnership.”

In addition to coordinating community-based testing, Unidos En Salud’s Clinical Response Team, based at ZSFG Ward 86, also offered ongoing medical screening and links to primary care, food assistance and other benefits to those who have tested positive, to enable them to self-isolate. The San Francisco Department of Public Health conducted contact tracing to identify individuals in the community who might have been exposed and needed support to safely quarantine.

Rapid analysis of nearly 4000 nasal swab tests was made possible by greatly increased capacity for COVID-19 sample analysis now available at a UCSF diagnostic laboratory adjacent to CZ Biohub at Mission Bay. That lab, built from scratch under DeRisi’s leadership in just eight days in March, was made possible in partnership with the Chan Zuckerberg Initiative.

The Unidos En Salud initiative is part of the recently launched UCSF COVID-19 Community Public Health Initiative. Led by Kirsten Bibbins-Domingo, PhD, MD, MAS, vice dean for population health and health equity at the UCSF School of Medicine, the initiative focuses on communities and populations disproportionately affected by the virus, and on building durable community partnerships.

In addition to COVID-19 testing, UCSF’s closely coordinated response to COVID-19 with the City and County of San Francisco, other Bay Area communities, and the state of California has included providing forecasts about the pandemic across the state and advice and counsel on pandemic response by UCSF epidemiologists; implementing a statewide contact tracing program in collaboration with the California Department of Health; providing $1 million and clinical expertise for the City to open a COVID-19 unit at Saint Francis Memorial Hospital; and opening a new, 53-bed respiratory isolation unit at UCSF Health’s Mount Zion hospital to expand the city’s overall hospital capacity for potential future surges, while offering dedicated space for current patients.

The proactive effort builds on UCSF’s long-standing commitment to addressing public health crises, which dates back to the University's founding in the mid-19th century, and includes such issues as homelessness, and such diseases as cholera, tuberculosis and HIV/AIDS.

Authors: See preprint for full listing of study authors. Authors were affiliated with UCSF, the Chan Zuckerberg Biohub, UC Berkeley, College of the Holy Cross, Unidos en Salud/United in Health, the Latino Task Force for COVID-19, and Abbott Laboratories.

Funding: The study was supported by the Chan Zuckerberg Biohub, UCSF, the Heising-Simons Foundation, and a Program for Breakthrough Biomedical Research award. ARCHITECT SARS-CoV-2 test kits were provided by Abbott Laboratories.

Disclosures: Co-authors Mary Rodgers and John Hackett Jr. work for Abbott Laboratories, which provided antibody test kits used in the study. Co-author Charles Chiu, MD, PhD, is the director of the UCSF-Abbott Viral Diagnostics and Discovery Center (VDDC) and receives research support funding from Abbott Laboratories.

The University of California, San Francisco (UCSF) is exclusively focused on the health sciences and is dedicated to promoting health worldwide through advanced biomedical research, graduate-level education in the life sciences and health professions, and excellence in patient care. UCSF Health, which serves as UCSF’s primary academic medical center, includes top-ranked specialty hospitals and other clinical programs, and has affiliations throughout the Bay Area.