Incubation periods of viral gastroenteritis: a systematic review

BMC Infectious Diseases

Derek AT Cummings²  Trish M Perl⁴  Nicholas G Reich³  Kara E Rudolph²  Rose A Lee¹  Justin Lessler²  Rachel M Lee¹ 

[1]Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, USA

[2]Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, USA

[3]Division of Biostatistics and Epidemiology, School of Public Health and Health Sciences, University of Massachusettes Amherst, Amherst, USA

[4]Department of Medicine, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, USA

关键词: Systematic review;    Astrovirus;    Caliciviruses;    Rotavirus;    Norovirus;    Incubation period;   

Others  :  1145727
DOI  :  10.1186/1471-2334-13-446

 received in 2013-03-06, accepted in 2013-09-12,  发布年份 2013

【 摘 要 】

Background

Accurate knowledge of incubation period is important to investigate and to control infectious diseases and their transmission, however statements of incubation period in the literature are often uncited, inconsistent, and/or not evidence based.

Methods

In a systematic review of the literature on five enteric viruses of public health importance, we found 256 articles with incubation period estimates, including 33 with data for pooled analysis.

Results

We fit a log-normal distribution to pooled data and found the median incubation period to be 4.5 days (95% CI 3.9-5.2 days) for astrovirus, 1.2 days (95% CI 1.1-1.2 days) for norovirus genogroups I and II, 1.7 days (95% CI 1.5-1.8 days) for sapovirus, and 2.0 days (95% CI 1.4-2.4 days) for rotavirus.

Conclusions

Our estimates combine published data and provide sufficient quantitative detail to allow for these estimates to be used in a wide range of clinical and modeling applications. This can translate into improved prevention and control efforts in settings with transmission or the risk of transmission.

【 授权许可】

   
2013 Lee et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI: Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 2003, 9:565-572.
• [2]Dennehy PH, Nelson SM, Spangenberger S, Noel JS, Monroe SS, Glass RI: A prospective case–control study of the role of astrovirus in acute diarrhea among hospitalized young children. J Infect Dis 2001, 184:10-15.
• [3]Herrmann JE, Taylor DN, Echeverria P, Blacklow NR: Astroviruses as a cause of gastroenteritis in children. N Engl J Med 1991, 324:1757-1760.
• [4]Kurtz J, Lee T: Astrovirus gastroenteritis age distribution of antibody. Med Microbiol Immunol 1978, 166:227-230.
• [5]Rodriguez-Baez N, O’Brien R, Qiu SQ, Bass DM: Astrovirus, adenovirus, and rotavirus in hospitalized children: prevalence and association with gastroenteritis. J Pediatr Gastroenterol Nutr 2002, 35:64-68.
• [6]Shastri S, Doane AM, Gonzales J, Upadhyayula U, Bass DM: Prevalence of astroviruses in a children’s hospital. J Clin Microbiol 1998, 36:2571-2574.
• [7]Lewis DC, Lightfoot NF, Cubitt WD, Wilson SA: Outbreaks of astrovirus type 1 and rotavirus gastroenteritis in a geriatric in-patient population. J Hosp Infect 1989, 14:9-14.
• [8]Gray JJ, Wreghitt TG, Cubitt WD, Elliot PR: An outbreak of gastroenteritis in a home for the elderly associated with astrovirus type 1 and human calicivirus. J Med Virol 1987, 23:377-381.
• [9]Technical Fact Sheet. http://www.cdc.gov/norovirus/php/illness-outbreaks.html webcite
• [10]Dolin R: Noroviruses–challenges to control. N Engl J Med 2007, 357:1072-1073.
• [11]Howley P, Knipe D, Fields B: Field’s Virology, 5th edn. Philadelphia: Lippincott, Williams & Wilkins; 2007.
• [12]Lessler J, Brookmeyer R, Perl TM: An evaluation of classification rules based on date of symptom onset to identify health-care associated infections. Am J Epidemiol 2007, 166:1220-1229.
• [13]Grotto I, Huerta M, Balicer RD, Halperin T, Cohen D, Orr N, Gdalevich M: An outbreak of norovirus gastroenteritis on an Israeli military base. Infection 2004, 32:339-343.
• [14]Schmid D, Stuger HP, Lederer I, Pichler AM, Kainz-Arnfelser G, Schreier E, Allerberger F: A foodborne norovirus outbreak due to manually prepared salad, Austria 2006. Infection 2007, 35:232-239.
• [15]Kaplan JE, Feldman R, Campbell DS, Lookabaugh C, Gary GW: The frequency of a Norwalk-like pattern of illness in outbreaks of acute gastroenteritis. Am J Public Health 1982, 72:1329-1332.
• [16]Fraser C, Riley S, Anderson RM, Ferguson NM: Factors that make an infectious disease outbreak controllable. Proc Natl Acad Sci USA 2004, 101:6146-6151.
• [17]Fischer TK, Bresee JS, Glass RI: Rotavirus vaccines and the prevention of hospital-acquired diarrhea in children. Vaccine 2004, 22(Suppl 1):S49-S54.
• [18]Blacklow NR, Herrmann JE: Astrovirus gastroenteritis. Trans Am Clin Climatol Assoc 1995, 106:58-66. discussion 66–58
• [19]Reich NG, Perl TM, Cummings DA, Lessler J: Visualizing clinical evidence: citation networks for the incubation periods of respiratory viral infections. PLoS One 2011, 6:e19496.
• [20]Lessler J, Reich NG, Brookmeyer R, Perl TM, Nelson KE, Cummings DA: Incubation periods of acute respiratory viral infections: a systematic review. Lancet Infect Dis 2009, 9:291-300.
• [21]Heymann D: Control of Communicable Diseases Manual. 19th edition. Washington, DC: American Public Health Association; 2008.
• [22]Mandell G, Bennet J, Dolin R: Principles and practice of infectious diseases. Philadelphia: Churchill Livingstone; 2005.
• [23]Pickering L: Red Book: 2009 report of the Committee on Infectious Diseases. 28th edition. Elk Grove Village, IL: American Academy of Pediatrics; 2009. 225, 241-242, 576-579
• [24]Cowling BJ, Muller MP, Wong IO, Ho LM, Louie M, McGeer A, Leung GM: Alternative methods of estimating an incubation distribution: examples from severe acute respiratory syndrome. Epidemiology 2007, 18:253-259.
• [25]Reich NG, Lessler J, Cummings DA, Brookmeyer R: Estimating incubation period distributions with coarse data. Stat Med 2009, 28:2769-2784.
• [26]Sartwell PE: The distribution of incubation periods of infectious disease. Am J Hyg 1950, 51:310-318.
• [27]coarseDataTools: A collection of functions to help with analysis of coarsely observed data. http://cran.r-project.org/web/packages/coarseDataTools webcite
• [28]Kurtz JB, Lee TW, Craig JW, Reed SE: Astrovirus infection in volunteers. J Med Virol 1979, 3:221-230.
• [29]Midthun K, Greenberg HB, Kurtz JB, Gary GW, Lin FY, Kapikian AZ: Characterization and seroepidemiology of a type 5 astrovirus associated with an outbreak of gastroenteritis in Marin County, California. J Clin Microbiol 1993, 31:955-962.
• [30]Mitchell DK, Van R, Morrow AL, Monroe SS, Glass RI, Pickering LK: Outbreaks of astrovirus gastroenteritis in day care centers. J Pediatr 1993, 123:725-732.
• [31]Baron RC, Murphy FD, Greenberg HB, Davis CE, Bregman DJ, Gary GW, Hughes JM, Schonberger LB: Norwalk gastrointestinal illness: an outbreak associated with swimming in a recreational lake and secondary person-to-person transmission. Am J Epidemiol 1982, 115:163-172.
• [32]Becker KM, Moe CL, Southwick KL, MacCormack JN: Transmission of Norwalk virus during football game. N Engl J Med 2000, 343:1223-1227.
• [33]Dolin R, Blacklow NR, DuPont H, Formal S, Buscho RF, Kasel JA, Chames RP, Hornick R, Chanock RM: Transmission of acute infectious nonbacterial gastroenteritis to volunteers by oral administration of stool filtrates. J Infect Dis 1971, 123:307-312.
• [34]Gill ON, Cubitt WD, McSwiggan DA, Watney BM, Bartlett CL: Epidemic of gastroenteritis caused by oysters contaminated with small round structured viruses. Br Med J (Clin Res Ed) 1983, 287:1532-1534.
• [35]Hicks NJ, Beynon JH, Bingham P, Soltanpoor N, Green J: An outbreak of viral gastroenteritis following a wedding reception. Commun Dis Rep CDR Rev 1996, 6:R136-R139.
• [36]Hoebe CJ, Vennema H, de Roda Husman AM, van Duynhoven YT: Norovirus outbreak among primary schoolchildren who had played in a recreational water fountain. J Infect Dis 2004, 189:699-705.
• [37]Kuritsky JN, Osterholm MT, Greenberg HB, Korlath JA, Godes JR, Hedberg CW, Forfang JC, Kapikian AZ, McCullough JC, White KE: Norwalk gastroenteritis: a community outbreak associated with bakery product consumption. Ann Intern Med 1984, 100:519-521.
• [38]Linco SJ, Grohmann GS: The Darwin outbreak of oyster-associated viral gastroenteritis. Med J Aust 1980, 1:211-213.
• [39]Matshuhashi N, Nishi Y, Nagoshi D, Kanemoto H: A N: Epidemic entercolitis possibly as a result of Norwalk virus infection presenting as ischemic colitis . Dig Endosc 2003, 15:138-141.
• [40]Chandler B, Beller M, Jenkerson S, Middaugh J, Roberts C, Reisdorf E, Rausch M, Savage R, Davis J: Outbreaks of Norwalk-like viral gastroenteritis–Alaska and Wisconsin, 1999. MMWR Morb Mortal Wkly Rep 2000, 49:207-211.
• [41]Taylor JW, Gary GW Jr, Greenberg HB: Norwalk-related viral gastroenteritis due to contaminated drinking water. Am J Epidemiol 1981, 114:584-592.
• [42]de Wit MA, Widdowson MA, Vennema H, de Bruin E, Fernandes T, Koopmans M: Large outbreak of norovirus: the baker who should have known better. J Infect 2007, 55:188-193.
• [43]Dolin R, Reichman RC, Roessner KD, Tralka TS, Schooley RT, Gary W, Morens D: Detection by immune electron microscopy of the Snow Mountain agent of acute viral gastroenteritis. J Infect Dis 1982, 146:184-189.
• [44]Gaulin C, Frigon M, Poirier D, Fournier C: Transmission of calicivirus by a foodhandler in the pre-symptomatic phase of illness. Epidemiol Infect 1999, 123:475-478.
• [45]Gotz H, de Jong B, Lindback J, Parment PA, Hedlund KO, Torven M, Ekdahl K: Epidemiological investigation of a food-borne gastroenteritis outbreak caused by Norwalk-like virus in 30 day-care centres. Scand J Infect Dis 2002, 34:115-121.
• [46]Hirakata Y, Arisawa K, Nishio O, Nakagomi O: Multiprefectural spread of gastroenteritis outbreaks attributable to a single genogroup II norovirus strain from a tourist restaurant in Nagasaki, Japan. J Clin Microbiol 2005, 43:1093-1098.
• [47]Isakbaeva ET, Bulens SN, Beard RS, Adams S, Monroe SS, Chaves SS, Widdowson MA, Glass RI: Norovirus and child care: challenges in outbreak control. Pediatr Infect Dis J 2005, 24:561-563.
• [48]Kirking HL, Cortes J, Burrer S, Hall AJ, Cohen NJ, Lipman H, Kim C, Daly ER, Fishbein DB: Likely transmission of norovirus on an airplane, October 2008. Clin Infect Dis 2010, 50:1216-1221.
• [49]Marks PJ, Vipond IB, Carlisle D, Deakin D, Fey RE, Caul EO: Evidence for airborne transmission of Norwalk-like virus (NLV) in a hotel restaurant. Epidemiol Infect 2000, 124:481-487.
• [50]Marshall JA, Yuen LK, Catton MG, Gunesekere IC, Wright PJ, Bettelheim KA, Griffith JM, Lightfoot D, Hogg GG, Gregory J, et al.: Multiple outbreaks of Norwalk-like virus gastro-enteritis associated with a Mediterranean-style restaurant. J Med Microbiol 2001, 50:143-151.
• [51]Thornhill TS, Wyatt RG, Kalica AR, Dolin R, Chanock RM, Kapikian AZ: Detection by immune electron microscopy of 26- to 27-nm viruslike particles associated with two family outbreaks of gastroenteritis. J Infect Dis 1977, 135:20-27.
• [52]Truman BI, Madore HP, Menegus MA, Nitzkin JL, Dolin R: Snow Mountain agent gastroenteritis from clams. Am J Epidemiol 1987, 126:516-525.
• [53]Humphrey TJ, Cruickshank JG, Cubitt WD: An outbreak of calicivirus associated gastroenteritis in an elderly persons home. A possible zoonosis? J Hyg (Lond) 1984, 93:293-299.
• [54]Johansson PJ, Bergentoft K, Larsson PA, Magnusson G, Widell A, Thorhagen M, Hedlund KO: A nosocomial sapovirus-associated outbreak of gastroenteritis in adults. Scand J Infect Dis 2005, 37:200-204.
• [55]Usuku S, Kumazaki M, Kitamura K, Tochikubo O, Noguchi Y: An outbreak of food-borne gastroenteritis due to sapovirus among junior high school students. Jpn J Infect Dis 2008, 61:438-441.
• [56]Yamashita Y, Ootsuka Y, Kondo R, Oseto M, Doi M, Miyamoto T, Ueda T, Kondo H, Tanaka T, Wakita T, et al.: Molecular characterization of Sapovirus detected in a gastroenteritis outbreak at a wedding hall. J Med Virol 2010, 82:720-726.
• [57]Kapikian AZ, Wyatt RG, Levine MM, Black RE, Greenberg HB, Flores J, Kalica AR, Hoshino Y, Chanock RM: Studies in volunteers with human rotaviruses. Dev Biol Stand 1983, 53:209-218.
• [58]Morris CA, Flewett TH, Bryden AS, Davies H: Epidemic viral enteritis in a long-stay children’s ward. Lancet 1975, 1:4-5.
• [59]Rodriguez WJ, Kim HW, Brandt CD, Yolken RH, Richard M, Arrobio JO, Schwartz RH, Kapikian AZ, Chanock RM, Parrott RH: Common exposure outbreak of gastroenteritis due to type 2 rotavirus with high secondary attack rate within families. J Infect Dis 1979, 140:353-357.
• [60]Mitchell DK, Matson DO, Cubitt WD, Jackson LJ, Willcocks MM, Pickering LK, Carter MJ: Prevalence of antibodies to astrovirus types 1 and 3 in children and adolescents in Norfolk, Virginia. Pediatr Infect Dis J 1999, 18:249-254.
• [61]Oliver SL, Asobayire E, Dastjerdi AM, Bridger JC: Genomic characterization of the unclassified bovine enteric virus Newbury agent-1 (Newbury1) endorses a new genus in the family Caliciviridae. Virology 2006, 350:240-250.
• [62]Scipioni A, Mauroy A, Vinje J, Thiry E: Animal noroviruses. Vet J 2008, 178:32-45.
• [63]Norovirus. http://www.cdc.gov/norovirus/hcp/clinical-overview.html webcite
• [64]Kitajima M, Oka T, Haramoto E, Phanuwan C, Takeda N, Katayama K, Katayama H: Genetic diversity of genogroup IV noroviruses in wastewater in Japan. Lett Appl Microbiol 2011, 52:181-184.
• [65]Kitajima M, Oka T, Haramoto E, Takeda N, Katayama K, Katayama H: Seasonal distribution and genetic diversity of genogroups I, II, and IV noroviruses in the Tamagawa River, Japan. Environ Sci Technol 2010, 44:7116-7122.
• [66]Caul EO, Appleton H: The electron microscopical and physical characteristics of small round human fecal viruses: an interim scheme for classification. J Med Virol 1982, 9:257-265.
• [67]Kaplan JE, Gary GW, Baron RC, Singh N, Schonberger LB, Feldman R, Greenberg HB: Epidemiology of Norwalk gastroenteritis and the role of Norwalk virus in outbreaks of acute nonbacterial gastroenteritis. Ann Intern Med 1982, 96:756-761.
• [68]Chiba S, Nakata S, Numata-Kinoshita K, Honma S: Sapporo virus: history and recent findings. J Infect Dis 2000, 181(Suppl 2):S303-S308.
• [69]Dey SK, Phan TG, Nguyen TA, Nishio O, Salim AF, Yagyu F, Okitsu S, Ushijima H: Prevalence of sapovirus infection among infants and children with acute gastroenteritis in Dhaka City, Bangladesh during 2004–2005. J Med Virol 2007, 79:633-638.
• [70]Blacklow NR, Greenberg HB: Viral gastroenteritis. N Engl J Med 1991, 325:252-264.
• [71]Noel JS, Liu BL, Humphrey CD, Rodriguez EM, Lambden PR, Clarke IN, Dwyer DM, Ando T, Glass RI, Monroe SS: Parkville virus: a novel genetic variant of human calicivirus in the Sapporo virus clade, associated with an outbreak of gastroenteritis in adults. J Med Virol 1997, 52:173-178.
• [72]Bishop RF, Davidson GP, Holmes IH, Ruck BJ: Virus particles in epithelial cells of duodenal mucosa from children with acute non-bacterial gastroenteritis. Lancet 1973, 2:1281-1283.
• [73]Parashar UD, Gibson CJ, Bresse JS, Glass RI: Rotavirus and severe childhood diarrhea. Emerg Infect Dis 2006, 12:304-306.
• [74]Mackow E: Group B and C rotaviruses. In Infections of the Gastrointestinal Tract. Edited by Blaser M, Smith P, Ravdin J, Greenberg H, Guerrant RL. New York: Raven Press; 1995:983-1008.
• [75]Santos N, Hoshino Y: Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 2005, 15:29-56.
• [76]Rodriguez WJ, Kim HW, Arrobio JO, Brandt CD, Chanock RM, Kapikian AZ, Wyatt RG, Parrott RH: Clinical features of acute gastroenteritis associated with human reovirus-like agent in infants and young children. J Pediatr 1977, 91:188-193.
• [77]Brandt CD, Kim HW, Rodriguez WJ, Arrobio JO, Jeffries BC, Stallings EP, Lewis C, Miles AJ, Chanock RM, Kapikian AZ, Parrott RH: Pediatric viral gastroenteritis during eight years of study. J Clin Microbiol 1983, 18:71-78.
• [78]Edmonson LM, Ebbert JO, Evans JM: Report of a rotavirus outbreak in an adult nursing home population. J Am Med Dir Assoc 2000, 1:175-179.
• [79]Hrdy DB: Epidemiology of rotaviral infection in adults. Rev Infect Dis 1987, 9:461-469.
• [80]Griffin MR, Surowiec JJ, McCloskey DI, Capuano B, Pierzynski B, Quinn M, Wojnarski R, Parkin WE, Greenberg H, Gary GW: Foodborne Norwalk virus. Am J Epidemiol 1982, 115:178-184.
• [81]Gunn RA, Janowski HT, Lieb S, Prather EC, Greenberg HB: Norwalk virus gastroenteritis following raw oyster consumption. Am J Epidemiol 1982, 115:348-351.
• [82]Malek M, Barzilay E, Kramer A, Camp B, Jaykus LA, Escudero-Abarca B, Derrick G, White P, Gerba C, Higgins C, et al.: Outbreak of norovirus infection among river rafters associated with packaged delicatessen meat, Grand Canyon, 2005. Clin Infect Dis 2009, 48:31-37.
• [83]Said MA, Perl TM, Sears CL: Healthcare epidemiology: gastrointestinal flu: norovirus in health care and long-term care facilities. Clin Infect Dis 2008, 47:1202-1208.
• [84]O’Ryan M, Linhares AC: Update on Rotarix: an oral human rotavirus vaccine. Expert Rev Vaccines 2009, 8:1627-1641.