Volume 21, Number 9—September 2015
THEME ISSUE
Emerging Infections Program
Emerging Infections Program
Emerging Infections Program—State Health Department Perspective
James L. Hadler
, Richard N. Danila, Paul R. Cieslak, James I. Meek, William Schaffner, Kirk E. Smith, Matthew L. Cartter, Lee H. Harrison, Duc J. Vugia, and Ruth Lynfield
, Richard N. Danila, Paul R. Cieslak, James I. Meek, William Schaffner, Kirk E. Smith, Matthew L. Cartter, Lee H. Harrison, Duc J. Vugia, and Ruth LynfieldAbstract
The Emerging Infections Program (EIP) is a collaboration between the Centers for Disease Control and Prevention and 10 state health departments working with academic partners to conduct active population-based surveillance and special studies for several emerging infectious disease issues determined to need special attention. The Centers for Disease Control and Prevention funds the 10 EIP sites through cooperative agreements. Our objective was to highlight 1) what being an EIP site has meant for participating health departments and associated academic centers, including accomplishments and challenges, and 2) the synergy between the state and federal levels that has resulted from the collaborative relationship. Sharing these experiences should provide constructive insight to other public health programs and other countries contemplating a collaborative federal–local approach to collective public health challenges.
In 1994, the Centers for Disease Control and Prevention (CDC) created the domestic Emerging Infections Program (EIP) as part of the response to the 1992 Institute of Medicine report recommending “the development and implementation of strategies that would strengthen state and federal efforts in U.S. surveillance” (1,2). The EIP was established as a collaborative population-based surveillance program involving CDC, selected state health departments, and their chosen academic institution partners. The major objective of the EIP was to conduct active population-based surveillance for a range of domestic emerging infectious diseases for which either no surveillance was occurring or state-level surveillance was occurring but “gold standard,” consistently high-quality surveillance was needed. The selected state health departments needed to engage clinical laboratories and infection control professionals throughout their jurisdictions. The relationship between CDC and the state health departments chosen to foster the EIP objectives has been a collaborative one, not purely a contractual relationship. Using a cooperative agreement funding mechanism, the federal, state, and academic collaborators have had shared responsibilities for setting priorities, planning and executing activities, and synthesizing and communicating results (3).
The infrastructure and expanded capacity that has resulted in terms of resources and collaborative relationships with CDC, between sites, and within each participating state have greatly enriched public health practice at each site and provided multiple state-based “laboratories” to pilot a variety of surveillance initiatives with possible national public health implications. The results have been remarkable: data to drive local and national public health initiatives have been gathered; state laboratory capacity to support surveillance has been updated and expanded, providing a model for expansion in other states; health threats from emerging infectious diseases have been identified and brought to national attention, and their epidemiology has been described; new methods to conduct surveillance have been piloted and adopted; staff in academic centers have become involved in public sector public health practice and research and expanded on them; and training and practice opportunities for public health students—the future epidemiology workforce—have multiplied.
In this article, our objectives are to describe 1) highlights of what being an EIP site has meant for participating health departments and associated academic centers, including accomplishments and challenges, and 2) the synergy between the state and federal levels that has resulted from the collaborative relationship. We hope that sharing these experiences will provide constructive insights to other public health program areas and other countries that are contemplating a collaborative national–local approach to collective public health challenges.
Several critical state-level, surveillance-related infrastructural enhancements have resulted from being an EIP site. First, federal EIP funding has been substantial. In 2014, EIP sites received an average of $3.6 million for personnel (including indirect costs), laboratory support, and supplies for all EIP projects in which they participated. This funding paid for a range of staff members, from 22 full-time equivalent (FTE) persons (spread over 27 positions) in the site with the smallest amount of personnel support to 58 FTEs (spread over 80 positions) in the site with the highest level of personnel support. The FTEs included staff in collaborating academic centers but excluded students in training positions.
Having additional epidemiology staff made it possible to conduct gold-standard surveillance for all diseases of EIP interest, with routine auditing of laboratories becoming an accepted feature of laboratory surveillance, thereby ensuring as close to 100% reporting from laboratories as possible. The experience and contacts from these efforts have made it possible for those running programs for non-EIP diseases (e.g., HIV, tuberculosis, sexually transmitted infections) to incorporate audits into their surveillance activities.
The additional resources, also made possible expansion of laboratory capacity to support surveillance. Additional staff enabled processing and storage of specimens of organisms from persons with invasive pneumococcal disease, group A Streptococcus (GAS) disease, and bacterial foodborne illness to enable typing and antimicrobial susceptibility testing, critical to the expanded surveillance role EIP sites have served for these infections. Updated laboratory capacity to perform pulsed-field gel electrophoresis enabled the EIPs to be in the forefront of identifying and investigating foodborne pathogen clusters and methicillin-resistant Staphylococcus aureus (MRSA) strains (4–7).
Second, incorporating laboratories, hospital infection prevention and control staff, and infectious disease physicians into the EIP sites by actively seeking their support and developing ways to share the information gathered from active surveillance has resulted in truly collaborative networks in each EIP site. Interest is such that in many sites EIP updates are a routine feature of grand rounds in some hospitals. Such interactions have resulted in more efficient and effective networks for communication and data dissemination, more efficient surveillance, and a sense of partnership among many of those involved (e.g., public health professionals, infectious disease clinicians, infection control practitioners, laboratorians) in contributing toward emerging infections work. These networks were used effectively during 2001–2003, before bioterrorism-related preparedness funding became available to support extensive communication systems in all states.
Third, in 2010, the EIPs began to conduct surveillance for health care–associated infections. Addition of capacity in this area has enabled EIP sites to move beyond encouraging hospitals to enroll in the National Healthcare Safety Network and produce annual reports of infection rates by hospital. EIP sites have established systems for ascertaining the number of central line–associated bloodstream infections within their entire catchment populations. Associated validation studies have identified limitations of definitions and enabled more complete case ascertainment. Methods have been established to enable estimation of the total number of nosocomial infections among hospitalized patients, setting the stage for repeated estimation to monitor trends over time (8). Interventions have been developed and studied for their effectiveness in some sites through communitywide collaboration.
Collaborations with academic health centers have enabled much greater flexibility in the types of surveillance and special studies that the EIPs and, correspondingly, the respective state health departments can undertake. These collaborations not only provide ready access to students looking to participate in research and public health practice projects but also provide easier access for hiring staff for specific short-term projects, making special risk factor studies easier to conduct. In addition, academic center–based staff can conduct intensive surveillance in smaller catchment areas, and interested faculty can collaborate in and enhance population-based surveillance research projects, including tying them into their clinical networks and efforts to seek funding. In Connecticut, for example, faculty from the Yale School of Medicine have taken advantage of, become involved in, and enhanced EIP surveillance for ehrlichiosis, neonatal sepsis, group A GAS disease, chronic liver disease, and precancerous cervical lesions caused by human papillomavirus (HPV) infection; they also have contributed to design and analysis of studies of the effectiveness of pneumococcal, rotavirus, and HPV vaccines. Infectious disease faculty and fellows at the Oregon Health and Science University have contributed to Oregon’s studies of Clostridium difficilediarrhea, emerging Cryptococcus gattii infections, nontuberculous mycobacterial infections, and surveillance and control of carbapenem-resistantEnterobacteriaceae. In Minnesota, collaborations with investigators at the University of Minnesota have enabled studies such as the assessment of variant influenza, matching of antimicrobial-resistant bacteria causing infections in animals with those causing infections in humans, and MRSA infections. In Tennessee, fellows and faculty from the Vanderbilt University School of Medicine have used local EIP data in studies of racial, geographic, and socioeconomic differences in the distribution of pneumococcal serotypes causing invasive disease, group A GAS intracranial infections, invasive pneumococcal infections in patients with sickle cell disease, neonatal early-onset group B Streptococcus (GBS) disease, and hospitalizations for influenza. The training relationship established between the Tennessee Department of Health and Vanderbilt University led directly to the prompt recognition and investigation of a recent large, multistate outbreak of fungal meningitis caused by a contaminated injectable steroid product. In Maryland, faculty from Johns Hopkins University designed and led a multisite study using EIP data on risk factors for invasive meningococcal disease among high school students.
Being an EIP site has meant conducting surveillance and obtaining local data for diseases for which the site was not previously conducting surveillance, implementing and evaluating prevention activities that could be or were being used without evaluation by other states, and using the data to reinforce existing or establishing new local disease control guidance. Diseases with new surveillance data for local use have included neonatal GBS and MRSA infections, invasive GAS disease and pneumococcal disease, non-O157 Shiga toxin–producing Escherichia coli (STEC), hospitalizations for influenza, C. difficile diarrhea (community- and health care–associated), and precancerous lesions caused by HPV infection. Diseases with data that have enabled local reinforcement and enhancement of prevention efforts include neonatal GBS, meningococcal disease, pneumococcal disease, influenza, salmonellosis, and HPV infection. As a result of having and using these data at a local level, EIP sites have become a resource to other states about how such data can be used.
The state-based EIP sites have contributed to the larger EIP in more ways than conducting the agreed-upon surveillance projects and special studies that have provided national-level data leading to new understanding and prevention initiatives on many fronts (3). In particular, these sites have been a source of ideas to be considered for new priority EIP projects, multiple and often independent “laboratories” for working out surveillance methods to meet changing needs, an attraction for local academic center staff to become involved and generate spin-off studies, and sources for training of future public health practitioners.
Innovation
The EIP has a Steering Committee comprising representation from CDC, participating state health departments, and their academic partners from all sites that meets at least annually to discuss administrative matters, progress, and future scientific direction. Although CDC staff usually lead the discussion, goals and priorities are determined collaboratively. Projects originally proposed by EIP sites that have shaped EIP priorities include surveillance for community-associated MRSA (1996 Steering Committee meeting), surveillance for community-associated C. difficile infections (2006 FoodNet Steering Committee meeting), and routine analysis of data using area-based socioeconomic measures (2012 Steering Committee meeting). These ideas cut across internal CDC boundaries at the time they were proposed. MRSA and C. difficile infections had been largely considered nosocomial problems, housed in CDC’s Division of Healthcare Quality Promotion. Initially, finding the right group at CDC to take an interest in the community perspective proved challenging. Measurement and ongoing monitoring of health conditions and risk factors incorporating measures of socioeconomic status other than race/ethnicity was neither centralized nor a routine concern for most CDC infectious disease programs. As a result, the Steering Committee established a Health Equity Working Group to develop standards and set the agenda for incorporating measures of socioeconomic status into routine EIP surveillance (9).
EIP sites also have piloted methods testing the feasibility of conducting population-based surveillance for new conditions and responding to changing laboratory technology. EIP sites piloted various forms of surveillance for community-associated MRSA for several years before settling on a common method (6,7,10,11). Collectively, a subset of sites piloted a standardized surveillance method for both community- and hospital-onset C. difficile infections, a successful endeavor that resulted in its becoming a core EIP surveillance project (12,13). Similarly, a subset of EIP sites piloted a standard method for surveillance for precancerous lesions for cervical cancer, demonstrating that the method was feasible. Surveillance for HPV cervical cancer precursors is now a core project for 5 EIP sites (14) and is contributing substantially in the assessment of the effectiveness of the vaccine at a population level. When some laboratories stopped performing cultures for E. coli O157 and switched to testing for Shiga toxin, the ability to detect outbreaks and monitor trends in E. coli O157 was threatened. A pilot project at an EIP site demonstrated the feasibility of turning this crisis into an opportunity to conduct surveillance for both non-O157 and O157 STEC by having the state laboratory culture all Shiga toxin–positive broths into which feces had been inoculated (15). Subsequently, surveillance for non-O157 STEC became part of core FoodNet surveillance, and these infections are proving to be even more common than infection by the prototypical E. coli O157 strain. Finally, the periodic EIP-sponsored FoodNet Population Surveys have measured frequencies of consumption of a variety of foods, including selected high-risk foods (e.g., alfalfa sprouts, unpasteurized milk). When such data were used in EIP sites as background rates in binomial probability calculations, they enabled rapid identification of food vehicles in outbreaks of salmonellosis, campylobacteriosis, and E. coli O157 infection (16–18). This method, coupled with confirmatory evidence from food tracebacks, case–control studies, or food testing, is now routinely used in many jurisdictions around the country (19–21).
Synergy
Collaborations with academic centers also have provided fertile ground for academic researchers to take advantage of the special surveillance projects being conducted in their midst to conduct spin-off projects, sometimes with funding from non-CDC sources. For example, in Connecticut, Yale University researchers have taken advantage of surveillance for ehrlichiosis, GAS, and HPV to conduct special studies beyond those commissioned through the EIP (22–26). Oregon’s high rates of disease caused by a clone of serogroup B Neisseria meningitidis led to a case–control study demonstrating a strong association with exposure to second-hand tobacco smoke (27) and to laboratory studies demonstrating the ability of N. meningitidis to alter its capsular polysaccharide (28). In Minnesota, academic partners have undertaken special studies of S. aureus (29) and GBS (30). In New York (Rochester) and Tennessee, the extent to which EIP surveillance for laboratory-confirmed influenza underestimated influenza-related hospitalizations in children was identified through collaboration and comparison with a research study with a different design than the EIP influenza surveillance (31).
EIP sites own their site-specific data and can conduct and publish analyses of these data independently of direct CDC involvement. This ownership has greatly expanded the dissemination of EIP surveillance findings (2 sites alone have published 151 local analyses of data in peer-reviewed publications [Technical Appendix[PDF - 416 KB - 18 pages]]). In addition, any site wanting to analyze all-site data can make a formal proposal to do so to the Steering Committee which if approved, gives it access to the de-identified all-site dataset (see Technical Appendix[PDF - 416 KB - 18 pages] for list of multisite publications led by 2 EIP sites). Overall, this flexibility has resulted not only in expanded dissemination of findings but also in expanded analytic creativity and data analysis capacity, and use of data for local and national purposes.
In another article in this issue, Vugia et al. have summarized the contribution of EIP sites to training of the current and future public health workforce (32). Although some training generated by EIP projects has occurred during the course of the CDC-based Epidemic Intelligence Service program and other CDC-based staff have gotten experience with data analysis, most training has occurred at the EIP sites as a result of the partnership in each site with an academic center. In 1 site alone, >190 students received training experiences during 1995–2014 (32). Of these, 75 students used their experience to fulfill thesis requirements, and 29 published an article in a peer-reviewed journal.
Although being an EIP site has provided multiple benefits for the state health department and academic center at each site, these benefits have come with some challenges. These challenges include data management; need for frequent human subjects committee reviews of special surveillance and nonsurveillance protocols, often by multiple institutions; and dedicated staff to manage complex budgets and contracts. The funding received by sites does not include the substantial in-kind resources necessary to conduct a large multicomponent program, which also must be integrated with existing public health programs.
EIP sites have found that conducting surveillance and research activities requires attention to the logistics of data acquisition, storage, and distribution. Increasing quantities of data have required development within EIP sites of expanded data storage and handling capacity and increased facility with data systems. Many sites have developed home-grown systems capable of gleaning data electronically, making the data available for epidemiologic analysis, while exporting required fields to CDC for multisite data aggregation. Such systems need built-in flexibility—for example, ready ability to add new conditions or variables of relevance to public health stemming from the sorts of emerging disease problems on which EIPs are called to address. Informatics expertise has proved essential.
In many sites, the EIP is the major source of protocols submitted to institutional review boards (IRBs). Whether a given EIP endeavor constitutes “research” meeting the federal definition (i.e., “designed to develop or contribute to generalizable knowledge” [33]) is not always clear because analysis of routinely collected surveillance data may provide knowledge that is, at least in some sense, generalizable. CDC routinely analyzes data generated by state public health agencies in the course of ascertaining and controlling reportable diseases to identify new risk factors and trends that may well be generalizable; not surprisingly, CDC and state health departments often have arrived at different determinations as to whether a given EIP activity constituted research. Moreover, some university collaborators consider any study in which its students are engaged to be research, requiring the protocol’s review by its IRB. The requirement that all IRBs approve the final protocol, and the multiplicity of IRBs (including those of individual hospitals, reviewing and imposing their own requirements on each protocol) for a 10-site EIP study involving university collaboration, can consume considerable time and effort.
With time, activities and expectations for EIPs have expanded, a fact welcomed by most sites. However, funding for the administrative work required by such expansions, including budget, contracts, and IRB tracking, and for hiring experienced epidemiologists to lead new projects has not always kept pace. EIPs note that funding increasingly must be directed to specified projects, leaving them with little flexibility and reduced ability to move beyond collecting data to writing articles for publication or crafting new protocols. As a consequence, such activities are increasingly left to CDC, jeopardizing some of the synergy of the collaborative partnership.
Given the challenges we describe and the frequent necessary coordination of surveillance and epidemiologic activities between local hospitals, laboratories, health departments, and state and federal partners, the structural setup that most EIP sites worked out is one in which the program is located within the lead state health department with or without a co-location within the lead partner school of public health or medicine.
The collaborative nature of the EIP has resulted in enhanced surveillance and laboratory capacity and communication networks in the 10 state public health departments. In addition, it has enriched research and public health training at the partner academic centers and produced synergy with the involved CDC programs, broadening the creativity and data analytic and dissemination capacity of all involved entities.
Dr. Hadler has worked with the EIP since its inception in 1995, first as the Connecticut State Epidemiologist and more recently based at the Yale School of Public Health, where he is Clinical Professor of Epidemiology. He was a member of the EIP Steering Committee during 1995–2008.
Acknowledgments
We acknowledge the contributions of the members of the EIP Steering Committee, past and present, for their collaborative work to make the EIP more than the sum of its component parts.
The work on this manuscript was supported by CDC Cooperative Agreement 5U50-CK000195.
References
- Institute of Medicine. Emerging infections: microbial threats to health in the United States. Washington, DC: National Academy Press; 1992 [cited 2015 Jun 25]. http://iom.edu/Reports/1992/Emerging-Infections-Microbial-Threats-to-Health-in-the-United-States.aspx
- Pinner RW. Addressing the challenges of emerging infectious disease. Am J Med Sci. 1996;311:3–8. DOIPubMed
- Pinner RW, Lynfield R, Hadler JL, Schaffner W, Farley MM, Frank ME, Cultivation of an adaptive domestic network for surveillance and evaluation of emerging infections. Emerg Infect Dis. 2015;9:1499–1509.
- Bender JB, Hedberg CW, Besser JM, Boxrud DJ, MacDonald KL, Osterholm MT. Surveillance for Escherichia coli O157:H7 infections in Minnesota by molecular subtyping. N Engl J Med. 1997;337:388–94. DOIPubMed
- Bender JB, Hedberg CW, Boxrud DJ, Besser JM, Wicklund JH, Smith KE, Use of molecular subtyping in surveillance for Salmonella enterica serotype Typhimurium. N Engl J Med. 2001;344:189–95. DOIPubMed
- Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Invasive methicillin-resistant Staphylococcus aureus infections in the United States.JAMA. 2007;298:1763–71. DOIPubMed
- Hadler JL, Petit S, Mandour M, Cartter ML. Trends in invasive infection with methicillin-resistant Staphylococcus aureus, Connecticut, USA, 2001–2010. Emerg Infect Dis. 2012;18:917–24 . DOIPubMed
- Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, Multistate point-prevalence survey of health care–associated infections. N Engl J Med. 2014;370:1198–208. DOIPubMed
- Hadler JL, Vugia DJ, Bennett NM, Moore MR. Minding the gaps: using the Emerging Infections Program to address health equity. Emerg Infect Dis.2015;9:1589–94.
- Morin CA, Hadler JL. Population-based incidence and characteristics of community-onset Staphylococcus aureus infections with bacteremia in 4 metropolitan Connecticut areas, 1998. J Infect Dis. 2001;184:1029–34. DOIPubMed
- Fridkin SK, Hageman JC, Morrison M, Sanza LT, Como-Sabetti K, Jernigan JA, Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med. 2005;352:1436–44. DOIPubMed
- Hirshon JM, Thompson AD, Limbago B, McDonald LC, Bonkosky M, Heimer R, Clostridium difficile infection in outpatients, Maryland and Connecticut, USA, 2002–2007. Emerg Infect Dis. 2011;17:1946–9. DOIPubMed
- Chitnis AS, Holzbauer SM, Belflower RM, Winston LG, Bamberg WM, Lyons C, Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011. JAMA Intern Med. 2013;173:1359–67. DOIPubMed
- Hariri S, Unger ER, Powell SE, Bauer HM, Bennett NM, Bloch KC, the HPV-IMPACT Working Group. The HPV vaccine impact monitoring project (HPV-IMPACT): assessing early evidence of vaccination impact on HPV-associated cervical cancer precursor lesions. Cancer Causes Control.2012;23:281–8. DOIPubMed
- Centers for Disease Control and Prevention. Laboratory-confirmed non-O157 Shiga toxin–producing Escherichia coli—Connecticut, 2000–2005.MMWR Morb Mortal Wkly Rep. 2007;56:29–31 .PubMed
- Centers for Disease Control and Prevention. Outbreak of Salmonella serotype Enteritidis infections associated with raw almonds—United States and Canada, 2003–2004. MMWR Morb Mortal Wkly Rep. 2004;53:484–7.
- Public Health Division, Oregon Department of Health Services. An outbreak of hemorrhagic escherichiosis traced to spinach. CD Summary2006;55:1–2 [cited 2015 Feb 27].https://public.health.oregon.gov/DiseasesConditions/CommunicableDisease/CDSummaryNewsletter/Documents/2006/ohd5523.pdf
- Lujan K, Cronquist A. Outbreak # 2009–43–001—Campylobacter outbreak associated with consumption of unpasteurized milk from a cow share operation, Montrose County 2009. State of Colorado report, November 6, 2009 [cited 2015 Feb 27].http://www.realrawmilkfacts.com/PDFs/Montrose-raw-dairy-report-Final.pdf
- Angelo KM, Chu A, Anand M, Nguyen TA, Bottichio L, Wise M, Outbreak of Salmonella Newport infections linked to cucumbers—United States, 2014. MMWR Morb Mortal Wkly Rep. 2015;64:144–7 .PubMed
- Slayton RB, Turabelidze G, Bennett SD, Schwensohn CA, Yaffee AQ, Khan F, Outbreak of Shiga toxin–producing Escherichia coli (STEC) O157:H7 associated with romaine lettuce consumption, 2011. PLoS ONE. 2013;8:e55300. DOIPubMed
- Centers for Disease Control and Prevention. Outbreak of Salmonella Heidelberg infections linked to a single poultry producer—13 states, 2012–2013. MMWR Morb Mortal Wkly Rep. 2013;62:553–6 .PubMed
- IJdo JW, Zhang Y, Hodzic E, Magnarelli LA, Wilson ML, Telford SR, The early humoral response in human granulocytic ehrlichiosis. J Infect Dis.1997;176:687–92. DOIPubMed
- Bessen DE, Izzo MW, Fiorentino TR, Caringal RM, Hollingshead SK, Beall B. Genetic linkage of exotoxin alleles and emm gene markers for tissue tropism in group A streptococci. J Infect Dis. 1999;179:627–36 . DOIPubMed
- Niccolai LM, McBride V, Julian PR. Sources of information for assessing human papillomavirus vaccination history among young women. Vaccine.2014;32:2945–7. DOIPubMed
- Niccolai LM, Mehta NR, Hadler JL. Racial/ethnic and poverty disparities in human papillomavirus vaccination completion. Am J Prev Med.2011;41:428–33. DOIPubMed
- Niccolai LM, Russ C, Julian PJ, Hariri S, Sinard J, Meek JI, Individual and geographic disparities in human papillomavirus types 16/18 in high-grade cervical lesions: associations with race, ethnicity and poverty. Cancer. 2013;119:3052–8. DOIPubMed
- Fischer M, Hedberg K, Cardosi P, Plikaytis BD, Hoesly FC, Steingart KR, Tobacco smoke as a risk factor for meningococcal disease. Pediatr Infect Dis J. 1997;16:979–83. DOIPubMed
- Swartley JS, Marfin AA, Edupuganti S, Liu LJ, Cieslak P, Perkins B, Capsule switching of Neisseria meningitidis. Proc Natl Acad Sci U S A.1997;94:271–6. DOIPubMed
- DeVries AS, Lesher L, Schlievert PM, Rogers T, Villaume LG, Danila R, Staphylococcal toxic shock syndrome 2000–2006: epidemiology, clinical features, and molecular characteristics. PLoS ONE. 2011;6:e22997. DOIPubMed
- Ferrieri P, Lynfield R, Creti R, Flores AE. Serotype IV and invasive group B Streptococcus disease in neonates, Minnesota, USA, 2000–2010. Emerg Infect Dis. 2013;19:551–8 .PubMed
- Grijalva CG, Weinberg GA, Bennett NM, Staat MA, Craig AS, Dupont WD, Estimating the undetected burden of influenza hospitalizations in children.Epidemiol Infect. 2007;135:951–8. DOIPubMed
- Vugia DJ, Meek JI, Danila RN, Jones TF, Schaffner W, Baumbach J, Training in infectious disease epidemiology through the Emerging Infections Program sites. Emerg Infect Dis. 2015;9:1516–19.
- Public Welfare. Protection of Human Subjects. 45 CFR §46 102(d). 2009.
Technical Appendix
Suggested citation for this article: Hadler JL, Danila RN, Cieslak PR, Meek JI, Schaffner W, Smith KE, et al. Emerging Infections Program—state health department perspective. Emerg Infect Dis. 2015 Aug [date cited]. http://dx.doi.org/10.3201/eid2109.150428
.png)
No hay comentarios:
Publicar un comentario