First Adenovirus to Jump Between Monkeys and Humans Confirmed
ScienceDaily (July 15, 2011) — A novel virus that spread through a California monkey colony in late 2009 also infected a human researcher and a family member, UCSF researchers have found, the first known example of an adenovirus "jumping" from one species to another and remaining contagious after the jump.
Adult Male Titi Monkey and his Infant at the California National Primate Research Center in Davis, California. A novel adenovirus species, named TMAdV (titi monkey adenovirus), was found to be the cause of a deadly pneumonia outbreak that killed more than one-third of the titi monkey colony and also infected a human scientist at the center. (Credit: Photograph courtesy of Kathy West)
In a study by the UCSF Viral Diagnostics and Discovery Center, which identified the new virus at the time of the outbreak, researchers confirmed it was the same virus in the New World titi monkeys and the two humans. They also confirmed that the virus is highly unusual in both populations, suggesting that it may have originated from a third, unidentified species.
The direction in which the virus spread, however -- from monkeys to humans or vice versa -- remains a mystery.
Findings appear in the July 14 issue of PLoS Pathogens, a weekly journal of the Public Library of Science.
Adenoviruses naturally infect many animals, including humans, monkeys and rodents, and are known to cause a wide range of clinical illnesses in humans, from cold-like symptoms to diarrhea and pneumonia. Unlike influenza or coronaviruses, adenoviruses had not been known to spread from one species to another.
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Cross-Species Transmission of a Novel Adenovirus Associated with a Fulminant Pneumonia Outbreak in a New World Monkey Colony
Eunice C. Chen1,2, Shigeo Yagi3, Kristi R. Kelly4, Sally P. Mendoza4, Nicole Maninger4, Ann Rosenthal4, Abigail Spinner4, Karen L. Bales4,5, David P. Schnurr3, Nicholas W. Lerche4, Charles Y. Chiu1,2,6*
1 Department of Laboratory Medicine, University of California San Francisco, San Francisco, California, United States of America, 2 UCSF-Abbott Viral Diagnostics and Discovery Center, University of California San Francisco, San Francisco, California, United States of America, 3 Viral and Rickettsial Disease Laboratory, California Department of Public Health, Richmond, California, United States of America, 4 California National Primate Research Center, University of California Davis, Davis, California, United States of America, 5Department of Psychology, University of California Davis, Davis, California, United States of America, 6 Department of Medicine, Division of Infectious Diseases, University of California San Francisco, San Francisco, California, United States of America
Abstract
Adenoviruses are DNA viruses that naturally infect many vertebrates, including humans and monkeys, and cause a wide range of clinical illnesses in humans. Infection from individual strains has conventionally been thought to be species-specific. Here we applied the Virochip, a pan-viral microarray, to identify a novel adenovirus (TMAdV, titi monkey adenovirus) as the cause of a deadly outbreak in a closed colony of New World monkeys (titi monkeys; Callicebus cupreus) at the California National Primate Research Center (CNPRC). Among 65 titi monkeys housed in a building, 23 (34%) developed upper respiratory symptoms that progressed to fulminant pneumonia and hepatitis, and 19 of 23 monkeys, or 83% of those infected, died or were humanely euthanized. Whole-genome sequencing of TMAdV revealed that this adenovirus is a new species and highly divergent, sharing <57% pairwise nucleotide identity with other adenoviruses. Cultivation of TMAdV was successful in a human A549 lung adenocarcinoma cell line, but not in primary or established monkey kidney cells. At the onset of the outbreak, the researcher in closest contact with the monkeys developed an acute respiratory illness, with symptoms persisting for 4 weeks, and had a convalescent serum sample seropositive for TMAdV. A clinically ill family member, despite having no contact with the CNPRC, also tested positive, and screening of a set of 81 random adult blood donors from the Western United States detected TMAdV-specific neutralizing antibodies in 2 individuals (2/81, or 2.5%). These findings raise the possibility of zoonotic infection by TMAdV and human-to-human transmission of the virus in the population. Given the unusually high case fatality rate from the outbreak (83%), it is unlikely that titi monkeys are the native host species for TMAdV, and the natural reservoir of the virus is still unknown. The discovery of TMAdV, a novel adenovirus with the capacity to infect both monkeys and humans, suggests that adenoviruses should be monitored closely as potential causes of cross-species outbreaks.
Author Summary
Infection from adenoviruses, viruses that cause a variety of illnesses in humans, monkeys, and other animals, has conventionally been thought to be species-specific. We used the Virochip, a microarray designed to detect all viruses, to identify a new species of adenovirus (TMAdV, or titimonkey adenovirus) that caused a deadly outbreak in a colony of New World titi monkeys at the California National Primate Research Center (CNPRC), and also infected a human researcher. One-third of the monkeys developed pneumonia and liver inflammation, and 19 of 23 monkeys died or were humanely euthanized. The unusually high death rate (83%) makes titi monkeys unlikely to be natural hosts for TMAdV, and the genomic sequence of TMAdV revealed that it is very different from any other known adenovirus. The researcher developed an acute respiratory illness at the onset of the outbreak, and was found to be infected by TMAdV by subsequent antibody testing. A clinically ill family member with no prior contact with the CNPRC also tested positive. Further investigation is needed to identify whether TMAdV originated from humans, monkeys, or another animal. The discovery of TMAdV suggests that adenoviruses should be monitored closely as potential causes of cross-species outbreaks.
Citation: Chen EC, Yagi S, Kelly KR, Mendoza SP, Maninger N, et al. (2011) Cross-Species Transmission of a Novel Adenovirus Associated with a Fulminant Pneumonia Outbreak in a New World Monkey Colony. PLoS Pathog 7(7): e1002155. doi:10.1371/journal.ppat.1002155
Editor: Glen R. Nemerow, The Scripps Research Institute, United States of America
Received: January 20, 2011; Accepted: May 23, 2011; Published: July 14, 2011
Copyright: © 2011 Chen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work is supported in part by CNPRC NIH grant NCRR P51-RR000169, NIH grant HD053555 (to KLB, SPM, and WAM), NIH grants K08-AI074913 and R56-AI089532 (to CYC), and an Abbott Viral Discovery Award (to CYC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors received a viral discovery award from Abbott Diagnostics (to CYC). The University of California, San Francisco (UCSF) has also filed a patent application related to TMAdV. This does not alter the authors' adherence to all PloS Pathogens policies on sharing data and materials.
* E-mail: charles.chiu@ucsf.edu
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