Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2016 Jan:86:104-19.
doi: 10.1016/j.mehy.2015.11.005. Epub 2015 Nov 6.

Seasonality and selective trends in viral acute respiratory tract infections

Patrick D Shaw Stewart  1
Affiliations

Seasonality and selective trends in viral acute respiratory tract infections

Patrick D Shaw Stewart. Med Hypotheses. 2016 Jan.

Abstract

Influenza A and B, and many unrelated viruses including rhinovirus, RSV, adenovirus, metapneumovirus and coronavirus share the same seasonality, since these viral acute respiratory tract infections (vARIs) are much more common in winter than summer. Unfortunately, early investigations that used recycled "pedigree" virus strains seem to have led microbiologists to dismiss the common folk belief that vARIs often follow chilling. Today, incontrovertible evidence shows that ambient temperature dips and host chilling increase the incidence and severity of vARIs. This review considers four possible mechanisms, M1 - 4, that can explain this link: (M1) increased crowding in winter may enhance viral transmission; (M2) lower temperatures may increase the stability of virions outside the body; (M3) chilling may increase host susceptibility; (M4) lower temperatures or host chilling may activate dormant virions. There is little evidence for M1 or M2, which are incompatible with tropical observations. Epidemiological anomalies such as the repeated simultaneous arrival of vARIs over wide geographical areas, the rapid cessation of influenza epidemics, and the low attack rate of influenza within families are compatible with M4, but not M3 (in its simple form). M4 seems to be the main driver of seasonality, but M3 may also play an important role.

PubMed Disclaimer

Figures

Fig. 1
Fig. 1
Graph II from van Loghem’s report on the epidemiology of vARIs in the Netherlands in the winter of 1925/26, with ambient temperature superimposed. The graph shows the percentages of persons with colds in seven regions of the Netherlands for 37 weeks. The data was compiled from the reports of 6933 correspondents that were submitted by post each week. Amsterdam had the largest number of informants (1159) and Noord-Holland the fewest (581). I have added the daily minimum outdoor air temperature (also averaged over 7 days at weekly intervals) from five Dutch weather stations, with the temperature scale inverted (lowest temperatures at the top). Note that by far the highest rate of vARIs was at the beginning of the study (September 1925), and that vARIs in different regions are closely correlated with each other and with inverted temperature. These correlations are strongest in the first half of the cold season. Correspondents reported coryza, angina, laryngitis, bronchitis and “influenza”. It is likely that a variety of viral “species” were present. See the main text for discussion of the events occurring during the intervals labeled i1, i2 and i3.
Fig. 2
Fig. 2
The Cirencester (UK) acute febrile respiratory diseases at 51.430 N, 1.590 W, compared with notifications of such diseases in Czechoslovakia (Prague, 50.050 N, 14-250 E), 1969–74, taken from Hope-Simpson’s investigation into the role of season in the epidemiology of influenza . This remarkable figure requires scientific explanation. The antigenic changes in influenza A virus (occurring at both sites) clearly show that novel influenza strains repeatedly moved across Europe during the period shown. There is, however, no evidence of moving “waves” of influenza because epidemics at the two sites are almost perfectly closely synchronized. Note that the shortest route between the two sites covers 1400 km by sea and road, crosses four national boundaries, and passes through some of the most densely-populated regions of Europe. This suggests that the virus moved to both sites prior to its manifestation, and a stimulus that was present at both sites triggered the concurrent epidemics. Bear in mind, however, that some influenza infections do not cause fevers. Influenza may have spread across Europe in the form of colds, before being strongly activated by low temperatures to yield febrile illness. These data are most readily explained by the fourth mechanism discussed below (M4), that virions can become dormant at some unknown location in the respiratory tract, and can subsequently be activated by host chilling. M3, which suggests that colder conditions weaken the immune defenses of hosts is also a possible explanation, but the very sudden onset of influenza in both locations is difficult to explain in this way.
Fig. 3
Fig. 3
Morbidity from colds in Cirencester, UK, 1954 and 1955, plotted alongside temperature . Thick line – percentage of volunteers showing symptoms. Thin line – earth temperature (inverted). See the main text for discussion of the events occurring during the intervals labeled i1 and i2.
Fig. 4
Fig. 4
The global distribution and seasonality of influenza and other vARIs, shown schematically. Time is indicated across the figure, while latitude is indicated from top to bottom. Levels of vARIs are indicated by brown shading, with dark brown showing the highest rates of infection. The figure shows general trends rather than specific data, but it is compatible with e.g. the Weekly Epidemiological Record of influenza A of the World Health Organization and other studies . The yellow curve shows the path of vertical solar radiation. The strange distribution of vARIs is shown, with more vARIs in the tropics throughout the year than in temperate regions during the summer months , , . It is known that seed strains of influenza A (H3N2) circulate continuously in a network in East and Southeast Asia (blue arrows) and spread to temperate regions from this network (green arrows) . Many studies show that personal chilling increases the prevalence of vARIs , , , , , , , , , and, since travel away from the tropical regions is associated with a decrease in temperature, it is likely that vARIs spread more quickly from the tropics to temperate regions (green arrows) than in the opposite direction (dotted red arrow). This is indeed the case for H3N2 influenza . The degree to which viruses remain dormant during the summer in temperate regions (dotted purple arrow) is unknown. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 5
Fig. 5
Chart 1 from Milam and Smillie’s 1929 study of colds on an isolated tropical island . The authors noted that outbreaks of colds often followed temperature drops, and were almost absent in the summer months. The red, green and blue bars indicate temperature fluctuations of 1.9, 1.5 and 1.0 °C respectively. (The large outbreak in December seems to have been introduced to the island by a sailor on the mail boat.). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 6
Fig. 6
The observed effect on temperature sensitivity of natural and (spontaneous) laboratory selection for increased and decreased viral activity. In this schematic 2-d plot the Xs indicate the starting levels of activity (virulence) and temperature sensitivity of two hypothetical viral strains. (The Xs could also indicate the properties of hypothetical viral proteins). Selective pressures are indicated by dotted arrows, while the resulting changes to viral phenotype are indicated by solid arrows. The establishment of persistent viral infections of cell cultures generally requires reduced viral activity so that viral and cell replication can be in balance , . The corresponding selective pressure is indicated by the dotted red arrow. Unexpectedly, reduced activity is often (though not always) accompanied by the spontaneous appearance of temperature (heat) sensitivity. This is indicated by the solid red arrow. See the main text for examples , , . The converse trend is equally surprising: when ts viruses are propagated in conditions that allow rapid growth (thereby selecting the most active mutants, dotted blue arrow), heat sensitivity has been lost (solid blue arrow) even when selection takes place at low temperatures (see main text [59], [74]). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Tamerius J., Nelson M.I., Zhou S.Z., Viboud C., Miller M.A., Alonso W.J. Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect. 2011;119(4):439. - PMC - PubMed
    1. Lofgren E., Fefferman N.H., Naumov Y.N., Gorski J., Naumova E.N. Influenza seasonality: underlying causes and modeling theories. J Virol. 2007;81(11):5429–5436. - PMC - PubMed
    1. Hope-Simpson R.E. Discussion on the common cold. Proc R Soc Med. 1958;51(4):267–271. - PMC - PubMed
    1. Du Prel J.B., Puppe W., Gröndahl B., Knuf M., Weigl F., Schaaff F. Are meteorological parameters associated with acute respiratory tract infections? Clin Infect Dis. 2009;49(6):861–868. - PubMed
    1. Van Loghem J.J. An epidemiological contribution to the knowledge of the respiratory diseases. J Hyg. 1928;28(01):33–54. - PMC - PubMed

LinkOut - more resources