Outbreak at Lake Qinghai

In May and June 2005, the HPAI H5N1 virus killed an unprecedented six thousand bar-headed geese near Lake Qinghai in western China [7], [9], which was later linked to outbreaks in Eurasia. While many aspects of avian influenza have been discussed, no study has considered the relationship among these events, the drop of temperature (down to −8°C), and the strong dust storms that occurred in the region during May 2–4, 2005 (Fig. S1 in Supporting information), the period in which the massive deaths of wild birds started.

In early May 2005, dust storms struck a wide area stretching from Mongolia to most of northwestern China (Figs. S1, S2, Table S1). These storms were caused by a swift-moving Siberian cold air mass that had channeled through valleys where several deserts locate (Fig. S2). Lake Qinghai, the site of the bar-headed goose deaths, is located about 500km east of the center of the Tsaidam Desert, where such large dust storms are rare [10]. However, it was at this time that strong wind stirred up a significant amount of dust locally. The cold air mass brought with it rapid temperature drops between the third and fifth of May, 2005, as recorded on the northern border of Lake Qinghai (Fig. 1a). On May 3, 4 and 5, temperatures dropped steeply from −0.4°C to −6.6°C and −8°C. Birds gathering around the lake, having just survived a long journey from southern China, then faced two major threats, i.e. subzero degrees temperatures and a sky filled with dust particles, simultaneously. Over the course of two to three days, these extreme and rapidly fluctuating conditions could have caused the birds enough physiological stress to suppress their immune systems [11]–[12]. Such two or three days of successive environmental stress and subsequent immunosuppression may have allowed the H5N1 virus to proliferate more efficiently in birds already carrying the virus, thereby increasing viral load and HPAI pathogenicity. These events would have hastened the inter-species spread of the virus and the deaths of wild birds over the following two months.

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Figure 1.

Variation of daily minimum temperatures at WMO stations near H5N1 virus outbreak areas. Each group and selected avian influenza H5N1 outbreaks events are listed in Table 1. Day 0 is the day with the lowest daily minimum temperature recorded; while the red dot represents the date of an outbreak of AIV was reported. For Figure 1(a) the day zero time point of group I was chosen as the time of the outbreak, not the time of the lowest temperature, since the former happened earlier.

https://doi.org/10.1371/journal.pone.0000191.g001

Outbreaks in Eurasia

Outbreaks of avian flu H5N1 in Europe came with similar changes in weather conditions. By tracking the dates and locations of HAPI H5N1 outbreaks in Eurasia between July 2005 and June 2006 and cross-referencing that information with meteorological data from local WMO stations, we observed a striking correlation. All of the 27 AIV H5N1 outbreaks listed in Table 1 coincided 100% with drops in temperature (Fig. 1). We then categorized these outbreaks into seven groups (I–VII) by geographical areas and dates of occurrence (Table 1), and found that outbreaks of AIV H5N1 occurred by 6 days later after “day 0”, a term used here to represent the day that lowest daily temperatures were reached (Fig. 1). Most were actually reported within the first three days after day 0, and some on day 0, itself. Below freezing temperatures, as low as −15.6°C, were recorded for four of the seven outbreak groups (I, III, IV and V); above freezing temperatures were recorded for the two other groups. Each of the outbreaks in these groups was officially announced after the discovery of deceased birds, which may mean that some of the outbreaks occurred earlier than they were officially reported. It, therefore, follows that practically all of the outbreaks of H5N1 we studied occurred during or immediately following the sudden and steep temperature drops.

Two of the outbreaks, marked by nearby dust storms, were peculiar to the May 4, 2005 and April 15, 2006 outbreaks at China's Qinghai Lake (in Groups I and VII, respectively). The dust storms combined with the quick temperature drops may have contributed to the spread of H5N1 in these areas.

After careful investigation of the composite plots of surface pressures, temperatures and wind flows on day 0 of each selected H5N1 outbreaks (Figs. S3, S4, S5, S6 and S7), the arrival of colder air from higher latitude region may be the main cause of the spread. Within two days, the daily minimum temperature can drop by 3 to 14°C, which varied by location and season. Outbreaks of H5N1 from Turkey to France between November 2005 and March 2006 (Groups IV and V) were found to have the most striking temperature drops.

Arrival of cold air mass

Most of the H5N1 outbreaks were associated with a Siberian cold air mass dominating Eurasia (Figs. S3, S4, S5, S6 and S7). This anticyclonic high pressure system moved southeastwardly transporting colder air on the eastern side of the system. The colder air flowed south toward the H5N1 outbreak area even during summer in southern Siberia (outbreaks II-a (Fig. S3), VII-d (Fig. S7)). In winter and spring, such high pressure system moved fast and brought below-freezing temperatures, termed widely as “cold air outbreak” events. On a few occasions, a portion of the cold air mass was separated from the main body and either became trapped in Turkey (outbreaks II-c (Fig. S3), IV-c and IV-e (Fig. S4)) or moved south to Egypt (outbreaks VI-a and VI-b (Fig. S7)), with much warmer temperatures than those reported in the northern areas from where the mass originated.

The occurrence of each of the lowest minimum temperatures was associated with both an arrival of cold air mass and an efficient radiative cooling under clear night-time skies. These conditions were sometimes followed by bright sunshine and air flows from a warmer region, resulting in a subsequent quick increase in temperature. In the outbreaks V-b and V-e, the temperatures increased by 11°C to 15°C just one day after day 0. H5N1 outbreaks were reported the next day. After examining the distribution of all the HPAI H5N1 outbreaks that occurred across many regions in the three major continents, the outbreaks indeed were associated with the very similar weather patterns as we mentioned above. Apparently, these dramatic weather fluctuations physically challenged the already fatigued migrating birds, just before official reports of avian flu outbreaks. This increased environmental stress is further strongly supported by the facts that HPAI H5N1 virus was detected in dead wild birds in even the more remote regions (outbreak VII-b) without poultry farms or trading centers [13].