Literature DB >> 23876187

Acute gastroenteritis surveillance through the National Outbreak Reporting System, United States.

Aron J Hall1, Mary E Wikswo, Karunya Manikonda, Virginia A Roberts, Jonathan S Yoder, L Hannah Gould.   

Abstract

Implemented in 2009, the National Outbreak Reporting System provides surveillance for acute gastroenteritis outbreaks in the United States resulting from any transmission mode. Data from the first 2 years of surveillance highlight the predominant role of norovirus. The pathogen-specific transmission pathways and exposure settings identified can help inform prevention efforts.

Entities:  

Keywords:  United States; acute gastroenteritis; bacteria; chemicals; enteric infections; foodborne disease; non-infectious causes; norovirus; outbreaks; parasites; pathogens; surveillance; toxins; viruses; waterborne disease

Mesh:

Year:  2013        PMID: 23876187      PMCID: PMC3739540          DOI: 10.3201/eid1908.130482

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


Acute gastroenteritis (AGE; defined as diarrhea or vomiting) is a major cause of illness in the United States; an estimated 179 million episodes occur annually (). AGE is caused by a variety of viral, bacterial, and parasitic pathogens and by toxins, chemicals, and other noninfectious causes. Noroviruses are the leading cause of epidemic gastroenteritis, detected in ≈50% of AGE outbreaks across Europe and the United States (,). However, until 2009, national surveillance for AGE outbreaks in the United States had been limited to foodborne or waterborne disease outbreaks because no national surveillance existed for AGE outbreaks spread by other transmission modes. To better understand and guide appropriate interventions to prevent epidemic gastroenteritis, the Centers for Disease Control and Prevention (CDC) launched a novel national surveillance system in 2009—the National Outbreak Reporting System (NORS). This system enhanced and expanded upon 2 existing surveillance systems, the Foodborne Disease Outbreak Surveillance System and the Waterborne Disease and Outbreak Surveillance System. NORS is an Internet-based system for local, state, and territorial health departments to report all outbreaks of foodborne and waterborne disease; AGE outbreaks caused by contact with infected persons, animals, or environmental sources; and AGE outbreaks caused by other or unknown modes of transmission (). As such, NORS provides a national surveillance system for all pathways of AGE outbreaks in the United States. To assess the roles of specific pathogens, temporal trends, and exposure pathways, we summarized AGE outbreak data submitted through NORS during the first 2 years after implementation of the system.

The Study

In the United States, outbreaks (defined as >2 cases of a similar illness epidemiologically linked to a common exposure, e.g., setting or food) can be reported through NORS by all 50 US states, the District of Columbia, US territories (American Samoa, Guam, Commonwealth of the Northern Mariana Islands, Puerto Rico, and the United States Virgin Islands), and Freely Associated States (Federated States of Micronesia, Republic of Marshall Islands, and Republic of Palau). NORS was launched in February 2009, but sites were encouraged to report outbreaks that occurred since January 1, 2009. For analysis, we extracted data reported through NORS for AGE outbreaks in which the symptom onset date for the first reported illness was during January 1, 2009–December 31, 2010. Outbreaks of diseases that do not typically cause AGE (e.g., listeriosis, legionellosis, hepatitis A) were excluded from analysis (). We analyzed various outbreak characteristics: date of first illness onset, primary transmission mode, confirmed or suspected etiology (), exposure setting, and number of outbreak-associated illnesses, hospitalizations, and deaths. Primary mode of transmission is determined by each reporting site on the basis of the local public health investigation and CDC guidance documents (). Of 4,455 outbreaks reported through NORS during 2009–2010, a total of 4,376 (98%) were AGE outbreaks (1,883 in 2009, 2,493 in 2010) (Table 1), associated with 122,488 reported illnesses, 2,952 hospitalizations, and 168 deaths. A single suspected or confirmed etiology was implicated in 2,819 (64%) outbreaks, associated with 88,958 (73%) illnesses, 2,381 (81%) hospitalizations, and 146 (87%) deaths. Norovirus, the leading cause of single-etiology outbreaks, was responsible for 1,908 (68%) outbreaks, associated with 69,145 (78%) illnesses, 1,093 (46%) hospitalizations, and 125 (86%) deaths. Salmonella spp., Shigella spp., and Shiga toxin–producing Escherichia coli (STEC), the next most frequently reported etiologic agents, were responsible for 355 (13%), 109 (4%), and 101 (4%) outbreaks, respectively. Salmonella spp. were the second most frequent cause of outbreak-associated hospitalizations (773 [32%]), and STEC was the second most frequent cause of outbreak-associated deaths (9 [6%]).
Table 1

Numbers of acute gastroenteritis outbreaks and outbreak-associated outcomes caused by various etiologic agents reported in the National Outbreak Reporting System, United States, 2009–2010*

Outbreak etiologyNo. (%) outbreaks
No. (%) outbreak-associated outcomes
ConfirmedSuspectedTotalIllnessesHospitalizationsDeaths
Single agent†
Norovirus‡1,355 (64.2)553 (78.1)1,908 (67.7)69,145 (77.7)1,093 (45.9)125 (85.6)
Salmonella spp.344 (16.3)11 (1.6)355 (12.6)8,590 (9.7)773 (32.5)6 (4.1)
Shigella spp.§99 (4.7)10 (1.4)109 (3.9)2,135 (2.4)115 (4.8)1 (0.7)
STEC88 (4.2)13 (1.8)101 (3.6)1,091 (1.2)250 (10.5)9 (6.2)
Campylobacter spp.¶56 (2.7)13 (1.8)69 (2.4)1,550 (1.7)52 (2.2)0
Clostridium spp.#41 (1.9)21 (3.0)62 (2.2)3,242 (3.6)16 (0.7)3 (2.1)
Cryptosporidium spp.**17 (0.8)30 (4.2)47 (1.7)598 (0.7)21 (0.9)1 (0.7)
Bacillus spp.††13 (0.6)12 (1.7)25 (0.9)522 (0.6)3 (0.1)0
Staphylococcus aureus11 (0.5)11 (1.6)22 (0.8)263 (0.3)00
Giardia intestinalis13 (0.6)6 (0.8)19 (0.7)121 (0.1)5 (0.2)0
Sc ombroid toxin/histamine18 (0.9)018 (0.6)76 (0.1)00
Ciguatoxin14 (0.7)014 (0.5)59 (0.1)6 (0.3)0
Rotavirus9 (0.4)5 (0.7)14 (0.5)372 (0.4)9 (0.4)0
Other‡‡
33 (1.6)
23 (3.2)
56 (2.0)

1,194 (1.3)
38 (1.6)
1 (0.7)
All single-agent etiologies2,111 (98.9)708 (31.6)2,819 (64.4)88,958 (72.6)2,381 (80.7)146 (86.9)
Multiple agents24 (1.1)9 (0.4)33 (0.8)1,236 (1.0)61 (2.1)2 (1.2)
Unknown agent01,524 (68.0)1,524 (34.8)32,294 (26.4)510 (17.3)20 (11.9)
All outbreaks2,135 (100.0)2,241 (100.0)4,376 (100.0)122,488 (100.0)2,952 (100.0)168 (100.0)

*STEC, Shiga toxin–producing Escherichia coli.
†Percentages for specific single agents are those among all single-agent etiology outbreaks (N = 2,819).
‡A norovirus genogroup was provided for 1,160 outbreaks: 150 GI, 1,003 GII, and 7 GI/GII. 
§S. sonnei (95 confirmed and 8 suspected outbreaks), S. flexneri (5 confirmed outbreaks), Shigella sp. not known (1 confirmed outbreak).
¶C. jejuni (55 confirmed and 4 suspected outbreaks), Campylobacter sp. not known (8 confirmed and 2 suspected outbreaks).
#C. perfringens (37 confirmed and 20 suspected outbreaks), Clostridium sp. not known (4 confirmed and 1 suspected outbreak).
**C. parvum (10 confirmed and 1 suspected outbreak), C. hominis (6 confirmed outbreaks), Cryptosporidium sp. not known (30 confirmed outbreaks).
††B. cereus (13 confirmed and 11 suspected outbreaks), Bacilllus sp. not known (1 suspected outbreak).
‡‡Includes Vibrio sp. (8 outbreaks), cyanobacterial toxins (6 outbreaks), enterotoxigenic and enteropathogenic E. coli (4 outbreaks), Enterococcus spp. (3 outbreaks), mycotoxins (3 outbreaks), Cyclospora spp. (2 outbreaks), pesticides (2 outbreaks), sapovirus (2 outbreaks), paralytic shellfish poison (1 outbreak), Pseudomonas sp. (1 outbreak), sodium hydroxide (1 outbreak), Yersinia sp. (1 outbreak), and other unspecified etiologies (22 outbreaks).

*STEC, Shiga toxin–producing Escherichia coli.
†Percentages for specific single agents are those among all single-agent etiology outbreaks (N = 2,819).
‡A norovirus genogroup was provided for 1,160 outbreaks: 150 GI, 1,003 GII, and 7 GI/GII. 
§S. sonnei (95 confirmed and 8 suspected outbreaks), S. flexneri (5 confirmed outbreaks), Shigella sp. not known (1 confirmed outbreak).
¶C. jejuni (55 confirmed and 4 suspected outbreaks), Campylobacter sp. not known (8 confirmed and 2 suspected outbreaks).
#C. perfringens (37 confirmed and 20 suspected outbreaks), Clostridium sp. not known (4 confirmed and 1 suspected outbreak).
**C. parvum (10 confirmed and 1 suspected outbreak), C. hominis (6 confirmed outbreaks), Cryptosporidium sp. not known (30 confirmed outbreaks).
††B. cereus (13 confirmed and 11 suspected outbreaks), Bacilllus sp. not known (1 suspected outbreak).
‡‡Includes Vibrio sp. (8 outbreaks), cyanobacterial toxins (6 outbreaks), enterotoxigenic and enteropathogenic E. coli (4 outbreaks), Enterococcus spp. (3 outbreaks), mycotoxins (3 outbreaks), Cyclospora spp. (2 outbreaks), pesticides (2 outbreaks), sapovirus (2 outbreaks), paralytic shellfish poison (1 outbreak), Pseudomonas sp. (1 outbreak), sodium hydroxide (1 outbreak), Yersinia sp. (1 outbreak), and other unspecified etiologies (22 outbreaks). AGE outbreaks were reported by the District of Columbia, Puerto Rico, and all states except Delaware (Figure 1). A median of 42 outbreaks (range 2–331) was reported by each site, and the median rate was 7.3 outbreaks/1 million person-years (range 0.9–44.8). Overall, AGE outbreaks exhibited winter seasonality: 2,972 (68%) of the 4,376 outbreaks occurred during November–April (Figure 2). This trend was driven largely by outbreaks caused by norovirus and by unknown etiologies, of which 1,530 (80% of 1,908 total) and 1,086 (71% of 1,524 total), respectively, occurred during November–April. In contrast, 62% of outbreaks caused by other etiologies, primarily bacteria, occurred during May–October.
Figure 1

Total number and annual rate of reported acute gastroenteritis outbreaks per 1 million population by reporting state, National Outbreak Reporting System, United States, 2009–2010. The number given in each state indicates the total number of outbreaks over the 2-year study period; the shading denoted by the legend indicates the reporting rate by quartiles. Multistate outbreaks (n = 48) and those reported by Puerto Rico (n = 15) and the District of Columbia (n = 24) are not shown.

Figure 2

Number of reported acute gastroenteritis outbreaks by month of first illness onset and etiology, National Outbreak Reporting System, United States, 2009–2010. *Includes outbreaks caused by a single etiologic agent other than norovirus or multiple etiologies.

Total number and annual rate of reported acute gastroenteritis outbreaks per 1 million population by reporting state, National Outbreak Reporting System, United States, 2009–2010. The number given in each state indicates the total number of outbreaks over the 2-year study period; the shading denoted by the legend indicates the reporting rate by quartiles. Multistate outbreaks (n = 48) and those reported by Puerto Rico (n = 15) and the District of Columbia (n = 24) are not shown. Number of reported acute gastroenteritis outbreaks by month of first illness onset and etiology, National Outbreak Reporting System, United States, 2009–2010. *Includes outbreaks caused by a single etiologic agent other than norovirus or multiple etiologies. The primary reported mode of transmission in most AGE outbreaks was person to person (2,271 [52%]), followed by foodborne (1,513 [35%]), waterborne (65 [2%]), animal contact (44, 1%), and environmental contamination (9, 0.2%); the transmission mode was unknown in 474 (10%) outbreaks (Table 2). Person-to-person transmission was implicated in most outbreaks caused by norovirus (1,261 [66%]) and Shigella spp. (86 [79%]), whereas foodborne transmission was implicated in most outbreaks caused by Salmonella spp. (254 [72%]) and STEC (64 [63%]). Among the 3,052 (70%) AGE outbreaks for which a single exposure setting was reported, health care facilities, primarily nursing homes, were the most frequent settings (1,499 [49%]), followed by restaurants or banquet facilities (657 [22%]), schools or day-care facilities (290 [10%]), and private residences (227 [7%]). Most norovirus outbreaks (64%) occurred in health care facilities, whereas shigellosis outbreaks (74%) occurred predominantly in schools or day-care facilities. Private residences and restaurants/banquet facilities were the most frequent exposure settings for outbreaks caused by Salmonella spp. (32% and 36%, respectively) and STEC (46% and 20%, respectively).
Table 2

Primary transmission mode and exposure setting of acute gastroenteritis outbreaks, by etiologic agent, National Outbreak Reporting System, United States, 2009–2010*

Outbreak characteristicNo. (%) outbreaks
Norovirus, n = 1,908Salmonella spp., n = 355Shigella spp., n = 109STEC, n = 101Other, n = 379†Unknown, n = 1,524Total, N = 4,376
Primary transmission mode
Person to person1,261 (66.1)17 (4.8)86 (78.9)11 (10.9)47 (12.4)849 (55.7)2,271 (51.9)
Foodborne494 (25.9)254 (71.5)8 (7.3)64 (63.4)220 (58.0)473 (31.0)1,513 (34.6)
Waterborne4 (0.2)02 (1.8)6 (5.9)51 (13.5)2 (0.1)65 (1.5)
Animal contact026 (7.3)05 (5.0)12 (3.2)1 (0.1)44 (1.0)
Environmental contamination5 (0.3)2 (0.6)1 (0.9)001 (0.1)9 (0.2)
Unknown
144 (7.5)
56 (15.8)
12 (11.0)
15 (14.9)
49 (12.9)
198 (13.0)
474 (10.8)
Exposure setting‡
Health care facility932 (48.8)5 (1.4)0025 (6.6)537 (35.2)1,499 (34.3)
Restaurant or banquet facility287 (15.0)69 (19.4)5 (4.6)12 (11.9)77 (20.3)207 (13.6)657 (15.0)
School or day-care facility98 (5.1)14 (3.9)50 (45.9)6 (5.9)15 (4.0)107 (7.0)290 (6.6)
Private residence31 (1.6)62 (17.5)4 (3.7)28 (27.7)60 (15.8)42 (2.8)227 (5.2)
Other single setting114 (6.0)42 (11.8)9 (8.3)15 (14.9)101 (26.6)98 (6.4)379 (8.7)
Multiple33 (1.7)19 (5.4)13 (11.9)10 (9.9)10 (2.6)21 (1.4)106 (2.4)
Not reported264 (13.8)86 (24.2)15 (13.8)15 (14.9)42 (11.8)313 (20.5)735 (16.8)
Not collected§149 (7.8)58 (16.3)13 (11.9)15 (14.9)49 (12.9)199 (13.1)483 (11.0)

*Data include both suspected and confirmed etiologies. STEC, Shiga toxin-producing Escherichia coli. 
†Includes outbreaks caused by a single etiologic agent other than norovirus, Salmonella spp., Shigella spp., and STEC or by multiple etiologic agents, as listed in Table 1.
‡Data on specific settings are restricted to outbreaks with a single exposure setting; for foodborne outbreaks, setting refers to the setting where implicated food was consumed.
§The setting was systematically not collected for outbreaks caused by environmental contamination or unknown transmission mode.

*Data include both suspected and confirmed etiologies. STEC, Shiga toxin-producing Escherichia coli. 
†Includes outbreaks caused by a single etiologic agent other than norovirus, Salmonella spp., Shigella spp., and STEC or by multiple etiologic agents, as listed in Table 1.
‡Data on specific settings are restricted to outbreaks with a single exposure setting; for foodborne outbreaks, setting refers to the setting where implicated food was consumed.
§The setting was systematically not collected for outbreaks caused by environmental contamination or unknown transmission mode.

Conclusions

As the national surveillance system for US AGE outbreaks, NORS provides valuable insights into the epidemiology of the pathogens most often involved. Building upon previous surveillance systems and analyses focused on specific transmission modes (–), NORS provides a more complete characterization of AGE outbreaks, particularly the relative importance of specific transmission modes and settings for the key pathogens. This analysis highlights norovirus as not only the leading cause of reported AGE outbreaks but also the leading cause of AGE outbreak–associated hospitalizations and deaths. Although norovirus usually causes self-limiting disease, it can cause severe outcomes when outbreaks occur among vulnerable populations, such as nursing-home residents (). Salmonella spp., Shigella spp., and STEC are also key contributors to AGE outbreaks. Expanded surveillance through NORS revealed that 28%, 91%, and 31%, respectively, of outbreaks caused by these 3 bacteria result from routes other than contaminated food or water. In addition, NORS provides information on non-AGE outbreaks transmitted by food or water. For example, ≈25% of waterborne disease outbreaks are caused by Legionella spp. (,), and among foodborne disease outbreaks, listeriosis is a major cause of outbreak-related hospitalizations and deaths (). As a passive reporting system, NORS is subject to variability in reporting practices between states and among outbreaks associated with different transmission modes and exposure settings. Reporting rates and data completeness may be improved through ongoing NORS enhancements, including direct data upload functionality and all-mode collection of setting information. For 35% of outbreaks, no suspected or confirmed etiology was identified, primarily because diagnostic specimens were not collected. However, outbreaks of unknown etiology exhibited similar temporal trends and epidemiologic characteristics as norovirus outbreaks, suggesting that many of these may have been caused by norovirus. NORS does not include AGE outbreaks on international cruise ships; however, if combined with the outbreaks reported to NORS, these cruise-ship outbreaks would represent <1% of all reported outbreaks attributed to norovirus and all-cause AGE (). Although a small minority of AGE cases in the United States are associated with reported outbreaks (≈1 in 3,000), outbreak surveillance provides unique insights that can inform prevention efforts. Norovirus control through hand hygiene, environmental disinfection, and isolation of ill persons should remain a priority and likely affords protection against other AGE agents (). Ongoing surveillance through NORS will help further elucidate trends, identify gaps, and assess the effects of future interventions on reducing epidemic gastroenteritis.
  10 in total

1.  Surveillance for waterborne disease outbreaks associated with drinking water---United States, 2007--2008.

Authors:  Joan M Brunkard; Elizabeth Ailes; Virginia A Roberts; Vincent Hill; Elizabeth D Hilborn; Gunther F Craun; Anu Rajasingham; Amy Kahler; Laurel Garrison; Lauri Hicks; Joe Carpenter; Timothy J Wade; Michael J Beach; Jonathan S Yoder Msw
Journal:  MMWR Surveill Summ       Date:  2011-09-23

2.  Surveillance for waterborne disease outbreaks and other health events associated with recreational water --- United States, 2007--2008.

Authors:  Michele C Hlavsa; Virginia A Roberts; Ayana R Anderson; Vincent R Hill; Amy M Kahler; Maureen Orr; Laurel E Garrison; Lauri A Hicks; Anna Newton; Elizabeth D Hilborn; Timothy J Wade; Michael J Beach; Jonathan S Yoder
Journal:  MMWR Surveill Summ       Date:  2011-09-23

Review 3.  Noroviruses: a comprehensive review.

Authors:  Manish M Patel; Aron J Hall; Jan Vinjé; Umesh D Parashar
Journal:  J Clin Virol       Date:  2008-12-11       Impact factor: 3.168

4.  Impact of an emergent norovirus variant in 2009 on norovirus outbreak activity in the United States.

Authors:  Catherine Yen; Mary E Wikswo; Ben A Lopman; Jan Vinje; Umesh D Parashar; Aron J Hall
Journal:  Clin Infect Dis       Date:  2011-08-10       Impact factor: 9.079

5.  Hospitalizations and mortality associated with norovirus outbreaks in nursing homes, 2009-2010.

Authors:  Tarak K Trivedi; Traci DeSalvo; Lore Lee; Aimee Palumbo; Maria Moll; Aaron Curns; Aron J Hall; Manish Patel; Umesh D Parashar; Benjamin A Lopman
Journal:  JAMA       Date:  2012-10-24       Impact factor: 56.272

6.  Outbreaks of acute gastroenteritis transmitted by person-to-person contact--United States, 2009-2010.

Authors:  Mary E Wikswo; Aron J Hall
Journal:  MMWR Surveill Summ       Date:  2012-12-14

7.  Updated norovirus outbreak management and disease prevention guidelines.

Authors: 
Journal:  MMWR Recomm Rep       Date:  2011-03-04

8.  Surveillance for foodborne-disease outbreaks--United States, 1998-2002.

Authors:  Michael Lynch; John Painter; Rachel Woodruff; Christopher Braden
Journal:  MMWR Surveill Summ       Date:  2006-11-10

9.  Foodborne illness acquired in the United States--unspecified agents.

Authors:  Elaine Scallan; Patricia M Griffin; Frederick J Angulo; Robert V Tauxe; Robert M Hoekstra
Journal:  Emerg Infect Dis       Date:  2011-01       Impact factor: 6.883

10.  Surveillance for foodborne disease outbreaks--United States, 2009-2010.

Authors: 
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2013-01-25       Impact factor: 17.586

  10 in total
  89 in total

Review 1.  Burden of norovirus in healthcare facilities and strategies for outbreak control.

Authors:  A Kambhampati; M Koopmans; B A Lopman
Journal:  J Hosp Infect       Date:  2015-02-04       Impact factor: 3.926

Review 2.  Norovirus Illnesses in Children and Adolescents.

Authors:  Minesh P Shah; Aron J Hall
Journal:  Infect Dis Clin North Am       Date:  2018-03       Impact factor: 5.982

3.  Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013.

Authors:  Everardo Vega; Leslie Barclay; Nicole Gregoricus; S Hannah Shirley; David Lee; Jan Vinjé
Journal:  J Clin Microbiol       Date:  2013-10-30       Impact factor: 5.948

4.  Foodborne Bacterial Pathogens Associated with the Risk of Gastroenteritis in the State of Qatar.

Authors:  Banjar Weam; Mariama Abraham; Sanjay Doiphode; Kenlyn Peters; Emad Ibrahim; Ali Sultan; Hussni O Mohammed
Journal:  Int J Health Sci (Qassim)       Date:  2016-04

Review 5.  Advances in laboratory methods for detection and typing of norovirus.

Authors:  Jan Vinjé
Journal:  J Clin Microbiol       Date:  2014-07-02       Impact factor: 5.948

6.  Genetic and Epidemiologic Trends of Norovirus Outbreaks in the United States from 2013 to 2016 Demonstrated Emergence of Novel GII.4 Recombinant Viruses.

Authors:  Jennifer L Cannon; Leslie Barclay; Nikail R Collins; Mary E Wikswo; Christina J Castro; Laura Cristal Magaña; Nicole Gregoricus; Rachel L Marine; Preeti Chhabra; Jan Vinjé
Journal:  J Clin Microbiol       Date:  2017-05-10       Impact factor: 5.948

Review 7.  Comprehensive review of human sapoviruses.

Authors:  Tomoichiro Oka; Qiuhong Wang; Kazuhiko Katayama; Linda J Saif
Journal:  Clin Microbiol Rev       Date:  2015-01       Impact factor: 26.132

8.  Salmonella enterica Serotype Newport Infections in the United States, 2004-2013: Increased Incidence Investigated Through Four Surveillance Systems.

Authors:  Stacy M Crim; Shua J Chai; Beth E Karp; Michael C Judd; Jared Reynolds; Krista C Swanson; Amie Nisler; Andre McCullough; L Hannah Gould
Journal:  Foodborne Pathog Dis       Date:  2018-07-23       Impact factor: 3.171

Review 9.  Treatment of norovirus infections: moving antivirals from the bench to the bedside.

Authors:  Stuart S Kaufman; Kim Y Green; Brent E Korba
Journal:  Antiviral Res       Date:  2014-02-25       Impact factor: 5.970

Review 10.  Infection control for norovirus.

Authors:  L Barclay; G W Park; E Vega; A Hall; U Parashar; J Vinjé; B Lopman
Journal:  Clin Microbiol Infect       Date:  2014-07-16       Impact factor: 8.067

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