Peer-Reviewed Journal Tracking and Analyzing Disease Trends pages 1497–1696 EDITOR-IN-CHIEF D. Peter Drotman Associate Editors EDITORIAL BOARD Paul Arguin, Atlanta, Georgia, USA Dennis Alexander, Addlestone, Surrey, UK Charles Ben Beard, Ft. Collins, Colorado, USA Timothy Barrett, Atlanta, Georgia, USA Ermias Belay, Atlanta, Georgia, USA Barry J. Beaty, Ft. Collins, Colorado, USA David Bell, Atlanta, Georgia, USA Martin J. Blaser, New York, New York, USA Sharon Bloom, Atlanta, GA, USA Christopher Braden, Atlanta, Georgia, USA Mary Brandt, Atlanta, Georgia, USA Arturo Casadevall, New York, New York, USA Corrie Brown, Athens, Georgia, USA Kenneth C. Castro, Atlanta, Georgia, USA Charles H. Calisher, Ft. Collins, Colorado, USA Louisa Chapman, Atlanta, Georgia, USA Michel Drancourt, Marseille, France Thomas Cleary, Houston, Texas, USA Paul V. Effler, Perth, Australia Vincent Deubel, Shanghai, China David Freedman, Birmingham, Alabama, USA Ed Eitzen, Washington, DC, USA Peter Gerner-Smidt, Atlanta, Georgia, USA Daniel Feikin, Baltimore, Maryland, USA Stephen Hadler, Atlanta, Georgia, USA Anthony Fiore, Atlanta, Georgia, USA Isaac Chun-Hai Fung, Statesboro, Georgia, USA Nina Marano, Nairobi, Kenya Kathleen Gensheimer, College Park, MD, USA Martin I. Meltzer, Atlanta, Georgia, USA Duane J. Gubler, Singapore David Morens, Bethesda, Maryland, USA Richard L. Guerrant, Charlottesville, Virginia, USA J. Glenn Morris, Gainesville, Florida, USA Scott Halstead, Arlington, Virginia, USA Patrice Nordmann, Fribourg, Switzerland Katrina Hedberg, Portland, Oregon, USA Didier Raoult, Marseille, France David L. Heymann, London, UK Pierre Rollin, Atlanta, Georgia, USA Charles King, Cleveland, Ohio, USA Ronald M. Rosenberg, Fort Collins, Colorado, USA Keith Klugman, Seattle, Washington, USA Frank Sorvillo, Los Angeles, California, USA Takeshi Kurata, Tokyo, Japan David Walker, Galveston, Texas, USA S.K. Lam, Kuala Lumpur, Malaysia Senior Associate Editor, Emeritus Stuart Levy, Boston, Massachusetts, USA Brian W.J. Mahy, Bury St. Edmunds, Suffolk, UK John S. MacKenzie, Perth, Australia Marian McDonald, Atlanta, Georgia, USA Managing Editor John E. McGowan, Jr., Atlanta, Georgia, USA Byron Breedlove, Atlanta, Georgia, USA Jennifer H. McQuiston, Atlanta, Georgia, USA Tom Marrie, Halifax, Nova Scotia, Canada Copy Editors Claudia Chesley, Laurie Dieterich, Karen Foster, Thomas Gryczan, Jean Michaels Jones, Shannon O’Connor, Nkuchia M. M’ikanatha, Harrisburg, Pennsylvania, USA Rhonda Ray, Carol Snarey, P. Lynne Stockton Philip P. Mortimer, London, UK Fred A. Murphy, Galveston, Texas, USA Production William Hale, Aaron Moore, Barbara Segal, Barbara E. Murray, Houston, Texas, USA Reginald Tucker P. Keith Murray, Geelong, Australia Stephen M. Ostroff, Silver Spring, MD, USA Editorial Assistant Jared Friedberg Ann Powers, Fort Collins, Colorado, USA Communications/Social Media Sarah Logan Gregory Gabriel Rabinovich, Buenos Aires, Argentina Mario Raviglione, Geneva, Switzerland Founding Editor David Relman, Palo Alto, California, USA Joseph E. McDade, Rome, Georgia, USA Connie Schmaljohn, Frederick, Maryland, USA Tom Schwan, Hamilton, Montana, USA Emerging Infectious Diseases is published monthly by the Centers for Disease Control and Ira Schwartz, Valhalla, New York, USA Prevention, 1600 Clifton Road, Mailstop D61, Atlanta, GA 30329-4027, USA. Telephone Tom Shinnick, Atlanta, Georgia, USA 404-639-1960, fax 404-639-1954, email [email protected]. Bonnie Smoak, Bethesda, Maryland, USA Rosemary Soave, New York, New York, USA The conclusions, findings, and opinions expressed by authors contributing P. Frederick Sparling, Chapel Hill, North Carolina, USA to this journal do not necessarily reflect the official position of the U.S. Depart- ment of Health and Human Services, the Public Health Service, the Centers for Robert Swanepoel, Pretoria, South Africa Disease Control and Prevention, or the authors’ affiliated institutions. Use of Phillip Tarr, St. Louis, Missouri, USA trade names is for identification only and does not imply endorsement by any of Timothy Tucker, Cape Town, South Africa the groups named above. Elaine Tuomanen, Memphis, Tennessee, USA All material published in Emerging Infectious Diseases is in the public John Ward, Atlanta, Georgia, USA domain and may be used and reprinted without special permission; proper J. Todd Weber, Atlanta, Georgia, USA citation, however, is required. Use of trade names is for identification only and does not imply Mary E. Wilson, Cambridge, Massachusetts, USA ∞ endorsement by the Public Health Service or by the U.S. Department of Health Emerging Infectious Diseases is printed on acid-free paper that meets the and Human Services. requirements of ANSI/NISO 239.48-1992 (Permanence of Paper) Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 September 2015 On the Cover Twenty Years of Active Bacterial Core Surveillance ........1520 Edward Middleton G. Langley et al. Manigault (1863–1923) This program has directly affected public health The Rocket, 1909. policies and practices. Oil on canvas, 20 × 24 in / 50.8 × 60.69 cm. Columbus The Foodborne Diseases Active Museum of Art, Ohio, USA; Surveillance Network—2 Decades of Museum Purchase, Achievements, 1996–2015 ........1529 Howald Fund II, 1981.009. O.L. Henao et al. FoodNet has provided a foundation for food About the Cover p. 1690 safety policy and illness prevention since 1996. Emerging Infections Evaluating Epidemiology and Program Improving Surveillance of Infections Associated with Emerging Infections Program— Health Care, United States ........1537 20 Years of Achievements and S.S. Magill et al. Future Prospects .......................1497 This national resource provides much-needed R. Lynfield and W. Schaffner data on pathogens, infections, and antimicrobial drug use. Cultivation of an Adaptive Domestic Network for The US Influenza Hospitalization Surveillance and Evaluation of Surveillance Network ................1543 Emerging Infections ..................1499 S.S. Chaves et al. R.W. Pinner et al. This network has helped determine risk, define Accomplishments of this program have p. 1500 severity, and guide recommendations for provided numerous dividends and might treatment and vaccination programs. benefit areas outside infectious diseases. Use of Pneumococcal Disease Emerging Infections Epidemiology to Set Policy Program—State Health and Prevent Disease during Department Perspective ............1510 20 Years of the Emerging J.L. Hadler et al. Infections Program ...................1551 This network has enriched research and p. 1530 M.R. Moore and C.G. Whitney workforce training and produced a synergy This program has been a flexible platform for between state and federal levels. following trends of this disease and evaluating vaccine effectiveness. Training in Infectious Disease Epidemiology through the Emerging Monitoring Effect of Human Infections Program Sites ...........1516 Papillomavirus Vaccines in US D.J. Vugia et al. Population, Emerging Infections EIP sites contribute substantially to Program, 2008–2012 ................1557 training current and future public S. Hariri et al. health professionals. Methods for surveillance of cervical precancers and associated types were developed to monitor effect of HPV vaccination. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 Emerging Infections Program September 2015 Improving Accuracy of Influenza- Associated Hospitalization Encephalitis Surveillance Rate Estimates ..........................1595 through the Emerging A.J. Millman et al. Infections Program, Adjusting for diagnostic test sensitivity 1997–2010 ..................1562 enables more accurate and timely K.C. Bloch and C.A. Glaser comparisons over time. A 3-state syndromic surveillance system documented reduction and emergence of Socioeconomic Disparities and neurologic infectious diseases. Influenza Hospitalizations, Tennessee, USA .........................1602 Tracking Pertussis and Evaluating C. Sloan et al. Control Measures through High rates of poverty, low education, and Enhanced Pertussis Surveillance, female single-parent households are Emerging Infections Program, associated with these hospitalizations. p. 1575 United States .............................1568 T.S. Skoff et al. Improved Phenotype-Based This program can improve pertussis Definition for Identifying prevention and control and be a model for Carbapenemase Producers surveillance programs. among Carbapenem-Resistant Enterobacteriaceae ...................1611 TickNET—A Collaborative Public N. Chea et al. Health Approach to Tickborne A new, less restrictive definition increases Disease Surveillance detection of Klebsiella pneumoniae and Research.............................1574 carbapenemase producers. P. Mead et al. Activities include burden-of-illness Socioeconomic Status and studies, high-quality prevention trials, and Foodborne Pathogens in pathogen discovery. Connecticut, USA, p. 1633 2000–2011 ................................1617 Emerging Infections Program B.M. Whitney et al. as Surveillance for Antimicrobial Diseases were associated with high Drug Resistance ........................1578 socioeconomic status and age of patient S.K. Fridkin et al. and serotype of organism. This program is a national resource for data on the epidemiology of antimicrobial drug–resistant Incidence of Clinician-Diagnosed infections and characteristics of isolates. Lyme Disease, United States, 2005–2010 ................................1625 Effect of Culture-Independent C.A. Nelson et al. Diagnostic Tests on Future Extrapolation from a large medical claims Emerging Infections database to the US population suggests that Program Surveillance ................1582 329,000 cases occur annually. G. Langley et al. Use of such tests in clinical settings presents Enhancing Lyme Disease opportunities and challenges. Surveillance by Using Administrative Claims Data, Emerging Infections Tennessee, USA ........................1632 Program Efforts to Address J.L. Clayton et al. Health Equity .............................1589 We identified 20% more cases, but the method J.L. Hadler at al. was resource intensive. The EIP has expanded efforts by using area-based socioeconomic analyses. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 1667 Follow-up of Contacts of Middle East Respiratory September 2015 Syndrome Coronavirus– Infected Returning Travelers, Emerging Infections the Netherlands, 2014 Program M. Mollers et al. 1515 Etymologia 1670 Reemergence and Surveillance Autochthonous Transmission of Dengue Virus, 1635 Photo Quiz Eastern China, 2014 W. Wang et al. Synopsis Letters 1674 Bidifobacterium breve Sepsis Mycobacterium abscessus in Child with High-Risk Acute Complex Infections Lymphoblastic Leukemia in Humans ...................1638 M.-R. Lee et al. 1675 Filovirus RNA in Fruit Bats, New treatments, rapid and inexpensive China p. 1662 identification methods, and measures to contain nosocomial transmission and 1677 Increase in Lymphadenitis outbreaks are urgently needed. Cases after Shift in BCG Vaccine Strain Dispatches 1679 Fatal Accelerated Cirrhosis after Imported HEV 1647 Putative Lineage of Novel Genotype 4 Infection African Usutu Virus, Central Europe 1681 Measles Reemergence in D. Cadar et al. Ceará, Northeast Brazil, 15 Years after Elimination 1651 Randomness of Dengue Outbreaks on the Equator 1683 Chikungunya Virus in Y. Chen et al. Macaques, Malaysia 1654 Acute Respiratory Infections p. 1680 1685 Functional Immune in Travelers Returning from Reconstitution by MERS-CoV–Affected Areas Interleuken-2 Adjunctive M. German et al. Therapy for HIV Mycobacterial Co-infection 1657 Third Wave of Influenza A(H7N9) Virus from Poultry, 1687 Corynebacterium bovis Guangdong Province, China, Eye Infections, Washington, 2014–2015 USA, 2013 S. Xie et al. About the Cover 1661 Disseminated Enteroviral Infection Associated with 1690 Ceaseless Experimentation Obinutuzumab Sparks Fireworks, Art, C. Dendle et al. and Science 1664 Laboratory Testing for Middle International Conference East Respiratory Syndrome on Emerging Infectious Coronavirus, California, USA, Diseases 2015 Poster and 2013–2014 Oral Presentation Abstracts M. Shahkarami et al. http://go.usa.gov/3AwnF Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 Presenting the ongoing challenges that emerging microbial threats pose to global health Emerging Infections Program— 20 Years of Achievements and Future Prospects Ruth Lynfield, William Schaffner “Disease-causing microbes have threatened human describes the considerable training and teaching activi- health for centuries. The Institute of Medicine’s ties undertaken by EIP investigators. Although training Committee on Emerging Microbial Threats to Health be- was among the consortium’s explicit goals when EIP was lieves that this threat will continue and may even intensify initiated, its funding has been evanescent, thus requiring in coming years” (1). Thus begins the Institute of Medi- commitment and imaginative flexibility to create train- cine’s 1992 Report on Emerging Infections. The Institute ing opportunities in the context of active investigations. of Medicine indicated that “emergence may be due to the However, EIP investigators have derived great pleasure in introduction of a new agent, to the recognition of an exist- training the next generation of public health epidemiolo- ing disease that has gone undetected, or to a change in the gists, and this has yielded dividends for mentees, mentors, environment that provides an epidemiologic bridge.” The and public health. recommendations encompassed both the ability to detect These initial articles are followed by a series of re- (surveillance) and respond to emerging infections. These views that summarize and assess core EIP areas and some recommendations laid the groundwork for establishment of related noteworthy projects. The network has successfully the Emerging Infections Program (EIP). established population-based surveillance for many patho- This issue of Emerging Infectious Diseases marks the gens of public health importance and has been able to pro- 20th anniversary of the EIP. Sponsored and organized by vide insights into risk factors for disease, and characteriza- the Centers for Disease Control and Prevention (CDC), tion of pathogens. EIP data have been used to inform public the EIP is a multifaceted collaboration of CDC with 10 health recommendations for the prevention and control of state health departments and their academic partners, with multiple infectious diseases and to evaluate public health the goal of conducting a portfolio of work that can be characterized as enhanced public health surveillance and Guest Editors applied research to detect, prevent, and control emerg- ing infectious diseases. Collaboration derives from the Dr. Lynfield is State Epidemiologist Latin word “collaboratus,” meaning to labor together. and Medical Director, Minnesota The collaboration has been profound and successful, with Department of Health, St. Paul. marked commitment, creativity, and passion contributed Minnesota. Her research interests by all participants. are emerging infectious diseases, This special issue incorporates a Festschrift for the antimicrobial resistance, and EIP, celebrating the accomplishments of this distinctive infection prevention. enterprise over the past 2 decades. The first article of the series uses a tree metaphor to describe the history of the EIP over the past 20 years and discusses future directions for the network. The following article provides a state- Dr. Schaffner is Professor of based perspective, which includes the enhancement of Preventive Medicine, Department of public health infrastructure and the development of new Health Policy and Professor of academic and public health partnerships. Another article Medicine, Division of Infectious Diseases, Vanderbilt University School Author affiliations: Minnesota Department of Health, St. Paul, of Medicine, Nashville, Tennessee. Minnesota, USA (R. Lynfield); Vanderbilt University School of His research interests are Medicine, Nashville, Tennessee, USA (W. Schaffner) communicable disease control and vaccine-preventable diseases. DOI: http://dx.doi.org/10.3201/eid2109.150564 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 1497 interventions. Not resting on their laurels, the authors of become true partners and value the mutual trust, sense of these articles also look to future challenges, including those harmony, and friendships that have flourished over the directly related to the infections, as well as others imposed years. These qualities, along with a shared commitment by health inequities and changes in technology. A series to science-based public health practice, have led to the of original research contributions by EIP investigators and success of the EIP and bode well as the network looks their collaborators follows the reviews. forward to tackling the next generation of emerging issues The scientific work of the EIP is directed through a of public health importance. genuinely collaborative steering committee comprised of lead investigators from all sites in the field, as well as Reference CDC. It is co-chaired by a CDC investigator and a site 1 Lederberg J, Shope RE, Oaks SC Jr, editors. Emerging infections: microbial threats to health in the United States. Washington (DC): senior investigator. Priority-setting discussions are open The National Academies Press; 1992 [cited 2015 Jun 18]. and genial, informed equally by national views and lo- http://www.nap.edu/catalog/2008/emerging-infections- cal perspectives. Formal votes are rare; consensus build- microbial-threats-to-health-in-the-united-states ing is the norm. The participants have longevity; many have been with the program since its inception and have Address for correspondence: Ruth Lynfield, Minnesota Department of nurtured it through 2 decades of administrative, fiscal, Health, 625 Robert St N, PO Box 64975, St. Paul, MN 55164, USA; and scientific labyrinths. As such, the participants have email: [email protected] March 2015: Tuberculosis Including: • Evaluation of the Benefits and Risks of Introducing Ebola Community Care Centers, Sierra Leone • N anomicroarray and Multiplex Next-Generation Sequencing for Simultaneous Identification and Characterization of Influenza Viruses • M ultidrug-Resistant Tuberculosis in Europe, 2010–2011 • R isk Factors for Death from Invasive Pneumococcal Disease, Europe, 2010 • M ycoplasma pneumoniae and Chlamydia spp. Infection in Community-Acquired Pneumonia, Germany, 2011–2012 • E pidemiology of Human Mycobacterium bovis Disease, California, USA, 2003–2011 • Regional Spread of Ebola Virus, West Africa, 2014 • Spillover of Mycobacterium bovis from Wildlife to Livestock, South Africa • Prisons as Reservoir for Community Transmission of Tuberculosis, Brazil • Polycystic Echinococcosis in Pacas, Amazon Region, Peru • Red Deer as Maintenance Host for Bovine Tuberculosis, Alpine Region http://wwwnc.cdc.gov/eid/articles/issue/21/3/table-of-contents 1498 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 Cultivation of an Adaptive Domestic Network for Surveillance and Evaluation of Emerging Infections Robert W. Pinner, Ruth Lynfield, James L. Hadler, William Schaffner, Monica M. Farley, Mark E. Frank, Anne Schuchat “The best time to plant a tree was 20 years ago; model for the EIP. Active surveillance and related research the second best time is now.” —Chinese Proverb conducted through collaborations between CDC and health departments generated information on the burden of and Through the metaphor of an adaptive, organic entity—a risk factors for toxic shock syndrome, listeriosis, Hae- tree with roots, a trunk, large limbs and smaller branch- mophilus influenzae type b (Hib) and group B Streptococ- es, fruits, and seeds (Figure 1)—this article describes the cus (GBS) infections, and meningococcal disease (3–6). Emerging Infections Program (EIP), reflects on this net- An earlier population-based active surveillance effort on work’s accomplishments over the past 20 years, and con- bacterial meningitis conducted in Bernalillo County, New siders opportunities and challenges for the future. Other Mexico, provided a similar model (7). The approach—pop- articles in this 2015 20th anniversary issue of Emerging ulation-based, active, laboratory-based surveillance, some- Infectious Diseases focusing on the EIP expand on many of times coupled with collection of disease-causing isolates the ideas introduced here, providing additional discussion, and always including key epidemiologic information—was details, and references. incorporated into today’s EIP activities. Whereas earlier activities focused on a single disease Roots or a small number of diseases and activities and operated The concepts of emerging infectious diseases are now fa- through contracts between CDC and health departments, miliar to the scientific community and the public. However, from the beginning the EIP dealt with multiple public health it took a 1992 Institute of Medicine report to emphasize the issues concurrently; engaged experts in state public health dynamic and modern factors that cause infectious diseases agencies, academic institutions, and a variety of CDC pro- to emerge and re-emerge and to put to rest the idea of infec- grams; and operated as a consortium in which stakeholders tious diseases as a solved problem, a worry for earlier times have mutual responsibilities for setting priorities, planning (1). The Centers for Disease Control and Prevention (CDC) and executing activities, and synthesizing and communi- Plan to Address Emerging Infections, released in April cating results (8,9). 1994, provided recommendations for action by CDC and other public health agencies (2). The CDC Plan highlighted Trunk the foundational role of surveillance and included in the Understanding the urgency, challenge, and complexity of recommendations creation of a network comprising state its mission and the need for a flexible model to support it, public health agencies, academic institutions, and CDC for the EIP built a network of collaborator sites, each contrib- special surveillance and applied public health research. The uting to shared governance, and established a strategic ap- EIP sprang from these recommendations. proach to guide projects. These elements serve as the trunk, Even before that time, active, population-based surveil- or supportive infrastructure, for EIP efforts. lance projects dating to the 1970s had provided a general The number of sites increased—from 4 in 1994 to the current number of 10 by 2002—as EIP activities demon- Author affiliations: Centers for Disease Control and Prevention, strated success, the need for broader geographic and de- Atlanta, Georgia, USA (R.W. Pinner, M.E. Frank, A. Schuchat); mographic representation was recognized, and funds be- Minnesota Department of Health, St. Paul, Minnesota, USA came available (Figure 2). EIP sites involve state health (R. Lynfield); Yale University School of Public Health, New Haven, department personnel and key collaborators in academic Connecticut, USA; (J.L. Hadler); Vanderbilt University School of institutions; each site engages others to conduct activities, Medicine, Nashville, Tennessee, USA (W. Shaffner); Emory including clinical laboratories and infection control pro- University School of Medicine, Atlanta (M.M. Farley) fessionals throughout each EIP area. The 10 EIP sites, to- DOI: http:;//dx.doi.org/10.3201/eid2109.150619 gether with several CDC programs and a coordinating unit Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015 1499 Figure 1. Structure and development of the Emerging Infections Program, United States. ABCs, Active Bacterial Core Surveillance; CDC, Centers for Disease Control and Prevention; IOM, Institute of Medicine; EI, emerging infections; HPV, human papillomavirus. at CDC, form the EIP network. EIP support comes from EIP activities. By the time of the Steering Group meeting in core funding intended to maintain and support the network November 1996, the group had adopted guiding principles and invest in key activities. In addition, other sources sup- and approved a framework for evaluating ideas for new proj- port specific EIP activities. For example, funding from the ects, which has guided assessment of potential new areas of US Department of Agriculture (USDA), the Food and Drug work and strategic directions (Table). Administration (FDA), and the Food Safety Initiative of Responsibilities and authorities are distributed across CDC have supported foodborne diseases work; the immu- the network’s membership. State public health agencies nization program of CDC supports vaccine effectiveness have legal authority for conducting surveillance; in this evaluation and related surveillance of vaccine-preventable context, academic partners function as agents of the state disease. Extramural funding for EIP cooperative agree- health departments. CDC has responsibility for expending ments has ranged from $2.3 million for 4 sites in 1995 to and managing federal funds invested in the EIP. Resources an average annual total of $33.8 million for the current 10 come from several funding streams, and each source requires sites during 2010–2014. accountability for ensuring that funds are spent well on ap- As early as the first EIP meeting in November 1994, propriate activities. This distribution of responsibilities and principals at CDC and EIP sites (including representatives authorities, coupled with the need for ensuring that the EIP from state health departments and academic partners) formed can respond nimbly to emerging issues, has meant that gov- an EIP Steering Group to provide guidance and strategy for ernance works flexibly, not rigidly—through negotiations 1500 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 9, September 2015