Volume 7, Number 3—June 2001
Seasonal Variation in Host Susceptibility and Cycles of Certain Infectious Diseases
|Pathogens peak at characteristic times in all seasons of the year||Winter: influenza, pneumococcus, rotavirus Spring: RSV, measles Summer: polio, other enteroviruses Fall: parainfluenza virus type 1|
|Timing and duration of peaks for each pathogen are similar from year to year||Measles: regular pattern since 1703 (1) Influenza: annual peak varies by only 5 to 10 weeks in the United States (6)|
|Onset of epidemics often occurs simultaneously in areas that are geographically dispersed and have different weather conditions and diverse populations||Influenza: simultaneous outbreaks across North America, 16 European countries, and 6 Chinese provinces (7) Pneumococcus: simultaneous outbreaks in seven surveillance areas (8)|
|Latitude is a critical determinant of timing and magnitude of peaks||An increasing magnitude of seasonal peaks as distance from the equator increases has been documented for polio (9) and rotavirus (10) and reported for influenza (11).|
|Pathogens can be detected in the off-season despite lower incidence of disease and virtual absence of epidemics||Meningococcus: no decrease in carriage in the off-season, despite absence of epidemic disease (12) RSV: sporadic summer viral isolation but no epidemic spread (13) Influenza: sporadic summer isolation, occasional clusters of disease without epidemic spread (14)|
RSV = respiratory syncytial virus. RSV peaks in the winter or spring in the United States, depending on location. For simplicity, it is listed here as a spring pathogen.
- Brownlee J. An investigation into the periodicity of measles epidemics in London from 1703 to the present day by the method of the periodogram. Philosophical Transactions of the Royal Society of London 1918;B 208:225-50.
- Anderson RM, Grenfell BT, May RM. Oscillatory fluctuations in the incidence of infectious disease and the impact of vaccination: time series analysis. J Hyg Camb. 1984;93:587–608.
- Riedo FX, Plikaytis B, Broome C. Epidemiology and prevention of meningococcal disease. Pediatr Infect Dis J. 1995;14:643–57.
- Witte JJ, Karchmer A, Case M, Herrmann KL, Abrutyn E, Kassanoff I, Epidemiology of rubella. Am J Dis Child. 1969;118:107–11.
- Török TJ, Kilgore PE, Clarke MJ, Holman RC, Bresee JS, Glass RI. Visualizing geographic and temporal trends in rotavirus activity in the United States, 1991 to 1996. National Respiratory and Enteric Virus Surveillance System Collaborating Laboratories. Pediatr Infect Dis J. 1997;16:941–6.
- Centers for Disease Control and Prevention. Update: Influenza activity--United States, 1999-2000 season. MMWR Morb Mortal Wkly Rep. 2000;49:173–7.
- Centers for Disease Control and Prevention. Update: Influenza activity--United States and worldwide, 1995-96 season, and composition of the 1996-97 influenza vaccine. MMWR Morb Mortal Wkly Rep. 1996;45:326–9.
- Dowell SF, Whitney C, Wright C, Schuchat A. Seasonal changes in invasive pneumococcal disease. Emerg Infect Dis. 2001. In press.
- Paccaud MF. World trends in poliomyelitis morbidity and mortality, 1951-1975. World Health Stat Q. 1979;32:198–224.
- Cook SM, Glass R, LeBaron C, Ho M-S. Global seasonality of rotavirus infections. Bull World Health Organ. 1990;68:171–7.
- Hope-Simpson RE, Golubev D. A new concept of the epidemic process of influenza A virus. Epidemiol Infect. 1987;99:5–54.
- Blakebrough IS, Greenwood B, Whittle H, Bradley A, Gilles H. The epidemiology of infections due to Neisseria meningitidis and Neisseria lactamica in a northern Nigerian community. J Infect Dis. 1982;146:626–37.
- Centers for Disease Control and Prevention. Update: respiratory syncytial virus activity - United States, 1998-1999 Season. MMWR Morb Mortal Wkly Rep. 1999;48:1104–15.
- Kohn MA, Farley T, Sundin D, Tapia R, McFarland L, Arden N. Three summertime outbreaks of influenza type A. J Infect Dis. 1995;172:246–9.
- Cox NJ, Fukuda K. Influenza. Infect Dis Clin North Am. 1998;12:27–38.
- Cox NJ, Subbarao K. Influenza. Lancet. 1999;354:1277–82.
- Langmuir AD, Schoenbaum S. The epidemiology of influenza. Hosp Pract. 1976;11:49–56.
- Hammond GW, Raddatz R, Gelskey D. Impact of atmospheric dispersion and transport of viral aerosols on the epidemiology of influenza. Rev Infect Dis. 1989;11:494–7.
- Kim PE, Musher D, Glezen W, Rodriguez-Barradas M, Nahm W, Wright C. Association of invasive pneumococcal disease with season, atmospheric conditions, air pollution, and the isolation of respiratory viruses. Clin Infect Dis. 1996;22:100–6.
- Checkley W, Epstein L, Gilman R, Figueroa D, Cama RI, Patz JA. Effects of El Niño and ambient temperature on hospital admissions for diarrheal diseases in Peruvian children. Lancet. 2000;355:442–50.
- Chew FT, Doraisingham S, Ling A, Kumarasinghe G, Lee B. Seasonal trends of viral respiratory tract infections in the tropics. Epidemiol Infect. 1998;121:121–8.
- Sung RY, Murray H, Chan R, Davies D, French G. Seasonal patterns of respiratory syncytial virus infection in Hong Kong: a preliminary report. J Infect Dis. 1987;156:527–8.
- Nathanson N, Martin J. The epidemiology of poliomyelitis: enigmas surrounding its appearance, epidemicity, and disappearance. Am J Epidemiol. 1979;110:672–92.
- Greenwood B. The epidemiology of acute bacterial meningitis in tropical Africa. Bacterial Meningitis. London: Academic Press; 1987. p. 61-91.
- Greenwood BM, Blakebrough I, Bradley A, Wali S, Whittle H. Meningococcal disease and season in sub-Saharan Africa. Lancet. 1984;i:1339–42.
- Diermayer M, Hedberg K, Hoesly F, Fischer M, Perkins B, Reeves M, Epidemic serogroup B meningococcal disease in Oregon: the evolving epidemiology of the ET-5 strain. JAMA. 1999;281:1493–7.
- D'Alessio D, Minor T, Allen C, Tsiatis A, Nelson D. A study of the proportions of swimmers among well controls and children with enterovirus-like illness shedding or not shedding an enterovirus. Am J Epidemiol. 1981;113:533–41.
- Hawley HB, Morin D, Geraghty M, Tomkow J, Phillips C. Coxsackievirus B epidemic at a boys' summer camp: isolation of virus from swimming water. JAMA. 1973;226:33–6.
- Hamer W. Epidemic disease in England--the evidence of variability and persistency of type. Lancet. 1906;11:733–9.
- Fine PE, Clarkson J. Measles in England and Wales - I: an analysis of factors underlying seasonal patterns. Int J Epidemiol. 1982;11:5–14.
- Rojansky N, Brzezinski A, Schenker J. Seasonality in human reproduction: an update. Hum Reprod. 1992;7:735–45.
- Wehr TA, Moul D, Barbato G, Giesen HA, Seidel JA, Barker C, Conservation of photoperiod-responsive mechanisms in humans. Am J Physiol. 1993;265:R846–57.
- Carlson LL, Zimmermann A, Lynch G. Geographic differences for delay of sexual maturation in Peromyscus leukopus: effects of photoperiod, pinealectomy, and melatonin. Biol Reprod. 1989;41:1004–13.
- Lincoln GA. Reproductive seasonality and maturation throughout the complete life-cycle in the mouflon ram (ovis musimon). Anim Reprod Sci. 1998;53:87–105.
- Rhind SM, McMillen S, Duff E, Hirst D, Wright S. Seasonality of meal patterns and hormonal correlates in red deer. Physiol Behav. 1998;65:295–302.
- Herndon JG, Bein M, Nordmeyer D, Turner J. Seasonal testicular function in male rhesus monkeys. Horm Behav. 1996;30:266–71.
- Chan PJ, Hutz R, Dukelow W. Nonhuman primate in vitro fertilization: seasonality, cumulus cells, cyclic nucleotides, ribonucleic acid, and viability assays. Fertil Steril. 1982;38:609–15.
- Löscher W, Fiedler M. The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. VI. Seasonal influences on maximal electroshock and pentylentetrazol seizure thresholds. Epilepsy Res. 1996;25:3–10.
- Sargeant JM, Shoukri M, Martin S, Leslie K, Lissemore K. Investigating potential risk factors for seasonal variation: an example using graphical and spectral analysis methods based on the production of milk components in dairy cattle. Prev Vet Med. 1998;36:167–78.
- Yellon SM, Fagoaga O, Nehlsen-Cannarella S. Influence of photoperiod on immune cell functions in the male Siberian hamster. Am J Physiol. 1999;276:R97–102.
- Demas GE, Nelson R. Exogenous melatonin enhances cell-mediated, but not humoral, immune function in adult male deer mice (Peromyscus maniculatus). J Biol Rhythms. 1998;13:245–52.
- Feigin RD, San Joaquin VH, Haymond MW, Wyatt RG. Daily periodicity of susceptibility of mice to pneumococcal infection. Nature. 1969;224:379–80.
- Shackelford PG, Feigin RD. Periodicity of susceptibility to pneumococcal infection: influence of light and adrenocortical secretions. Science. 1973;182:285–7.
- Wongwiwat M, Sukapanit S, Triyanond C, Sawyer WD. Circadian rhythm of the resistance of mice to acute pneumococcal infection. Infect Immun. 1972;5:442–8.
- Sack RL, Brandes R, Kendall A, Lewy A. Entrainment of free-running circadian rhythms by melatonin in blind people. N Engl J Med. 2000;343:1070–7.
- Sher L, Goldman D, Ozaki N, Rosenthal N. The role of genetic factors in the etiology of seasonal affective disorder. J Affect Disord. 1999;53:203–10.
- Eastman CI, Young M, Fogg L, Liu L, Meaden P. Bright light treatment of winter depression: a placebo-controlled trial. Arch Gen Psychiatry. 1998;55:883–9.
- Pell JP, Cobbe S. Seasonal variations in coronary heart disease. QJM. 1999;92:689–96.
- Ownby HE, Frederick J, Mortensen R, Ownby D, Russo J. Seasonal variations in tumor size at diagnosis and immunological responses in human breast cancer. Invasion Metastasis. 1986;6:246–56.
- Calvo JR, Rafil-El-Idrissi M, Pozo D, Guerrero J. Immunomodulatory role of melatonin: specific binding sites in human and rodent lymphoid cells. J Pineal Res. 1995;18:119–26.
- Boctor FN, Charmy R, Cooper E. Seasonal differences in the rhythmicity of human male and female lymphocyte blastogenic responses. Immunol Invest. 1989;18:775–84.
- Maes M, Stevens W, Scharpe S, Bosmans E, De Meyer F, D'Hondt P, Seasonal variation in peripheral blood leukocyte subsets and in serum interleukin-6, and soluble interleukin-2 and -6 receptor concentrations in normal volunteers. Experientia. 1994;50:821–9.
- Nelson RJ, Drazen D. Melatonin mediates seasonal adjustments in immune function. Reprod Nutr Dev. 1999;39:383–98.
- Paigen B, Ward E, Reilly A, Houten L, Gurtoo HL, Minowada J, Seasonal variation of aryl hydrocarbon hydroxylase activity in human lymphocytes. Cancer Res. 1981;41:2757–61.
- Shadrin AS, Marinich I, Taros L. Experimental and epidemiological estimation of seasonal and climato-geographical features of non-specific resistance of the organism to influenza. J Hyg Epidemiol Microbiol Immunol. 1977;21:155–61.
- Schulman JL, Kilbourne E. Experimental transmission of influenza virus infection in mice. II. Some factors affecting the incidence of transmitted infections. J Exp Med. 1963;118:267–75.
- Swartz TA, Skalska P, Gerichter C. Routine administration of oral polio vaccine in a subtropical area. Factors possibly influencing sero-conversion rates. J Hyg Camb. 1972;70:719–26.
- World Health Organization Collaborative Study Group on Oral Poliovirus V. Factors affecting the immunogenicity of oral poliovirus vaccine: a prospective evaluation in Brazil and the Gambia. J Infect Dis. 1995;171:1097–106.
- Deming MS, Linkins R, Jaitch K, Hull H. The clinical efficacy of trivalent oral polio vaccine in the Gambia by season of vaccine administration. J Infect Dis. 1997;175(suppl1):S254–7.
- Schonberger LB, McGowan JJ, Gregg M. Vaccine-associated poliomyelitis in the United States, 1961-1972. Am J Epidemiol. 1976;104:202–11.