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Influenza: probable primary spread triggered by the abiotic vehicle drinking wat

er
Abstract
The triggering of human influenza epidemics by biotic droplet infection is not p
roven and is improbable, because epidemics rarely arise together in recognizable
clusters and are caused by locally isolated virus subtypes and strains. These s
trains appear in a locally isolated pattern geographically, and have not been sh
own to arise primarily in large cities and densely populated areas, but have bee
n found predominantly in the colder regions of Germany, reaching their peak regu
larly in certain districts/cities. Moreover, the appearance of these strains run
s closely parallel to the course of winter cooling, and it is unlikely that they
spread via saliva droplets, since saliva contains far fewer influenza virus par
ticles than the heavier droplets from the throat and nose.
In temperate climates, the strict dependence on environmental temperatures makes
it improbable that the primary transmission of influenza occurs through warm bi
otic droplet infection. Influenza transmission must be triggered by an abiotic v
ehicle that is increasingly efficient in spreading infection with increasingly c
old environmental temperatures. Therefore, the question arises as to which abiot
ic vehicles are dependent on cold environmental temperatures for the transmissio
n of influenza. Drinking water is such an abiotic vehicle. This article shows th
at cold drinking water may be an abiotic vehicle through which virulent human in
fluenza viruses reach humans from infection reservoirs which is responsible pred
ominantly for triggering seasonal influenza epidemics. This also applies specifi
cally to the new H1N1 influenza virus with vomiting or/and diarrhoea and the let
hal H5N1 avian influenza virus, whose potential transmission via water is well e
stablished.

Background
a) Droplet infection, temperature and humidity: The triggering of human influenz
a epidemics by biotic droplet infection is unproven1. Lowen et al. have demonstr
ated that influenza virus transmission in a guinea pig model is most efficient u
nder cold and dry conditions2,3. A new study from Oregon, USA has described a co
rrelation between humidity and influenza virus survival and transmission. When a
bsolute humidity is low – as in the peak influenza months of January and February –
the virus appears to survive longer and transmission rates increase4,5.
b) Cluster: Influenza epidemics in Germany rarely occur together in recognizable
clusters, e.g., in only 15% of the cases during the 2006/2007 season6.
c) Influenza subtypes: The virus subtypes and strains involved in influenza epid
emics are locally isolated. This is one indicator for why a broad homogeneous ai
rborne “virus cloud” for the initial spread of influenza is unlikely.
d) Geographical allocation: The emergence of influenza epidemics shows a particu
lar and unexpected geographical pattern. They have not been shown to arise mainl
y in large cities and densely populated areas. They appear predominantly in the
colder regions of Germany, e.g., in the east in the winter with its cold contine
ntal climate, in the southeast, and at higher altitudes. They appear with maximu
m regularity in certain districts/cities.
e) Seasonal Influenza: An evident correlation can be observed between the parall
el trends of influenza epidemics and the course of winter cooling. The influenza
season starts and stops at a soil and water temperature of 7°C. Influenza inciden
ce correlates to a much greater extent with soil and water than air temperature.
Air temperature is an ad hoc indicator for frost and thaw. Soil and water tempe
ratures are long-term indicators for the course of winter cooling. Frost inhibit
s the input of secreted influenza viruses in water. Frost inhibited the start of
the influenza season in Germany in 2006. The differences in the extent of influ
enza epidemics in general can be explained by the increased use of analytical an
d rapid diagnostic tests, in particular since 2007, as a result of H5N1 avian in
fluenza in Europe in the winter of 2006. In 2006 a 7-week frost inhibited the st
art of the influenza season until mid-February. Also, the seasonal virus secrete
d from infected animals may play an important role in the differing extent of in
fluenza epidemics. In the next few years the epidemiological database will be mo
re comprehensive as a result of further increases in the use of rapid diagnostic
tests. Every year in colder Saxony, with 74% of its drinking water coming from
surface water, the influenza season is much more severe than in Germany as a who
le, where only 33% of the drinking water originates from surface water. Every ye
ar, as in week 11, 2007, the influenza peak in Saxony follows the thaw. Overall
in Germany, there was no marked frost in 2007. The soil curves for Germany and S
axony are very similar, considerably more so than the air curves. This is why we
have included the soil curve for Saxony.
f) Influenza transmission: The transmission routes for the common cold and influ
enza are still debatable. The commonly held belief is that colds are spread by p
articles of infected mucous generated by coughs and sneezes. Immunohistological
studies have shown that foci of virus-producing cells are clustered in the mucou
s layer of the respiratory tract. Infected persons can shed millions of virus pa
rticles in their mucus. However, there is increasing evidence that infection als
o occurs via contaminated surfaces and other abiotic vehicles. This can occur wh
en surfaces such as handkerchiefs and tissues, water taps, door handles or telep
hones become contaminated by droplets shed from the nose of infected individuals
. The virus is passed on to another person when they touch a contaminated surfac
e. Water is also an abiotic vehicle. It is not known which transmission routes a
re the most important9. From a biological point of view, influenza infection is
unlikely to be spread through saliva droplets, since saliva contains far fewer i
nfluenza virus particles than the substantially heavier droplets of mucus from t
he throat and nasal membranes10,11. Coughs and sneezes tend to spray saliva from
the pool at the front of the mouth rather than droplets of mucus from the throa
t and nose. Saliva contains little or no cold virus and thus aerosolized saliva
is unlikely to spread infection. Colds are not caught by kissing, as cold viruse
s do not infect the mouth and saliva contains very little virus. When volunteers
infected with the common cold kissed cold-free volunteers for up to 1.5 minutes
, only one case of cross-infection occurred in 16 trials12. Infected birds secre
te the influenza virus through their saliva, nasal secretions and feces. Avian i
nfluenza viruses have been isolated from unconcentrated lake water, which indica
tes that waterfowl have a very efficient way of transmitting viruses, i.e. via f
ecal material in the water supply13. Avian influenza viruses in wild aquatic bir
ds are spread by fecal-oral transmission through the water supply14. Initial tra
nsmission of avian influenza viruses to mammals, including pigs and horses, prob
ably also occurs by fecal contamination of water13. Shedding of the influenza vi
rus into water leads to transmission between waterfowl, and is a major threat fo
r epidemics in poultry and pandemics in humans15. A single human infectious dose
of seasonal influenza virus might be between 100 and 1000 particles16-19. As ex
pected, there are no data on the human infectious dose of influenza virus concer
ning contact with drinking water or contact between water and oral mucous membra
nes, conjunctiva, eardrums or wounds. The human infectious dose of H5N1 avian in
fluenza virus is also unknown.
g) Human influenza viruses in mammals: Human influenza viruses have been identif
ied in the excretions of mammals, such as pigs (fecal and oronasal), wild boar (
fecal and oronasal), cattle and goats. Hence in principle, from a virological po
int of view the transmission path from the environment to mammals and humans is
possible via water, especially drinking water13,20-30. Thus, it is highly probab
le that more animal species infected with influenza A will be discovered in futu
re13. In this way, human influenza viruses are secreted into the environment and
water. Secreted influenza virus titers are usually very high. Avian influenza v
iruses have been isolated from unconcentrated lake water, which indicates that h
uman influenza viruses can also be isolated from untreated water.

Effectiveness of elimination and inactivation of viruses during treatment of dri


nking water
To determine resistance of highly pathogenic H5N1 avian influenza virus to chlor
ination, Rice et al.31 exposed allantoic fluid that contained two virus strains
to chlorinated buffer at pH 7 and 8, at 5°C. They concluded that free chlorine con
centrations typically used in drinking water treatment were sufficient to inacti
vate the virus by more than three orders of magnitude. However, drinking water m
ay be colder than 5°C, e.g. 3°C. The pH value is often >8.0, e.g. 9.5. In the cold a
nd at high pH, virus inactivation by chlorine is rather poor. Rice et al.31 used
the maximum US chlorination level of 2.0 mg/L free chlorine. Only 0.1-0.3 mg/L
free chlorine are allowed in Germany. The performance levels of water treatment
units regarding virus inactivation32 are valid under the precondition that micro
organisms in water are in suspension, not embedded in particles32. In environmen
tal waters, secreted influenza viruses are always embedded in particles. Hence t
he demonstrated level of avian influenza virus inactivation in allantoic fluid d
iluted in buffer is not consistent with real conditions. Moreover, the WHO32 req
uires virus inactivation/filtration rates from six (surface water) to four (grou
ndwater) orders of magnitude. Rice et al.31 only demonstrated three orders of ma
gnitude. Hence the authors are not convinced that chlorinated water is safe. Rea
l worst-case conditions are cold drinking water at 3°C, pH 9.5, chlorination lower
than 2 mg/L (or no chlorination but filtration), perhaps 0.2 mg/L as in Germany
, influenza viruses embedded in particles, and required virus inactivation/filtr
ation performance from six to four orders of magnitude.
In Germany, drinking water is often only roughly filtered or not at all. Thus, v
ery small viruses are not filtered out reliably. In the treatment of groundwater
, the widespread filtration plants for the elimination of iron and manganese are
ineffective in eliminating viruses32. The goals demanded by the WHO regarding e
limination and inactivation of viruses cannot be met32, even in Germany, with it
s efficient plants for flocculation and filtration, and the common disinfection
procedures followed (chlorine, ozone treatment, and UV irradiation), whose effic
iency declines with decreasing water temperature (chlorine and ozone treatment),
because microorganisms clumped in water are only reduced to a limited extent.

"Cooling chain of the public water supply"


Coldness is the most important parameter for the preservation of virulent influe
nza viruses in water33-38. The minimum temperature of water in German reservoirs
is 3–5°C in the months of January and February. River water also reaches its minimu
m temperature in those months. Also, groundwater taken from deeper wells can be
colder if there is insufficient sealing between the well pipes and the surroundi
ng rocks. This allows the infiltration of surface water to influence the tempera
ture of the groundwater, which may make it colder than the deeper groundwater. M
oreover, surface water trickling from streams and arriving at the wells within s
hort distances can have the same effect. River bank filtrate pumped from wells t
hat are drilled near the bank takes on the temperature of the cold river water,
and the same applies to wells from which groundwater enriched with surface water
is pumped. The 1-m deep soil temperatures correspond to the temperatures of the
underground, frost-protected, drinking water pipelines. In Germany, the minimum
soil temperatures at a depth of 1 m are 3–5°C during February and March39. The temp
erature inside the drinking water pipelines and that of the drinking water trans
ported in them adapts to the soil temperature. In winter, cold, untreated water
arrives at the drinking-water treatment plants, and remains cold in the water ta
nks and pipelines after treatment, up to the houses of consumers. In particular,
the minimum temperature of tap water corresponds to the cold winter temperature
in the soil and water pipelines, and rises in February–March. Only at domestic ta
ps is the cold drinking water mixed with warm water from the house. This process
is the “cooling chain of the public water supply”, from the water source to the con
sumers, with a drinking water temperature of, for instance, 3–5°C in February–March. C
old, fresh drinking water taken from surface water, insufficiently protected gro
undwater near the surface, as well as groundwater from rocks contaminated by inf
luenza viruses, may be the abiotic vehicle that transports the virulent influenz
a viruses in winter at temperatures of 3–5°C. The viruses are conserved effectively
in the cold and transported to humans via the cooling chain of the public water
supply.

Transmission paths of drinking water - basic principle


Infections through drinking water are not only transmitted through drinking the
water, but also through the inhalation of aerosols during showers and contact wi
th drinking water. The entry sites in humans are the conjunctiva, nasal and oral
mucous membranes, eardrums, wounds, and contaminated catheters infecting other
mucous membranes.

Influenza transmission in temperate climates and tropical regions


In temperate regions, influenza epidemics recur with marked seasonality around t
he end of winter, in the northern as well as the southern hemisphere. Although s
easonality is one of the most familiar features of influenza, it is also one of
the least understood. Indoor crowding during cold weather, seasonal fluctuations
in host immune responses, and environmental factors, including relative humidit
y, temperature and UV radiation, have all been assumed to account for this pheno
menon, but none of these has been tested directly. Influenza also causes signifi
cant morbidity in tropical regions; however, in contrast to the situation in tem
perate zones, influenza in the tropics is not strongly associated with a certain
season.
In the tropics, clear links are observed between the cold rainy seasons, floods
and the spread of influenza. There is a widespread link between avian influenza
and water, e.g. in Egypt, with respect to the Nile delta, or in Indonesia, with
respect to the less prosperous residential districts with backyard flocks of bir
ds, and without a central water supply, as in Vietnam40. However, the direct bio
tic transmission from birds, poultry or humans to humans cannot be dependent on
the cold rainy seasons or floods. Water is a very efficient abiotic vehicle for
the spread of viruses – in particular, the fecal viruses, as well as those excrete
d through the mouth, nose and eyes. Infected humans, mammals, birds and poultry
can contaminate drinking water everywhere, and all humans require water frequent
ly and have very intensive contact with water in general, and not only through d
rinking.
The virulence of influenza viruses depends on the temperature and time. Especial
ly in cases of local water supplies freshly contaminated with influenza virus fr
om wells near the surface, cisterns, tanks, rain barrels, ponds, rivers, or rice
paddies, this pathway can explain the small clusters in households. For example
, at 24°C in the tropics, the virulence of influenza viruses in water persists onl
y for 2 days. However, in temperate climates with central water supplies, the te
mperature of the “older”, less fresh contaminated water is decisive for virus virule
nce. At 7°C, the influenza virus virulence in water extends to 14 days.
Ducks and rice paddies may be critical factors in spreading avian influenza41. D
ucks, rice paddies and people, but not chickens, have emerged as the most signif
icant factors in the spread of avian influenza in Thailand and Vietnam42. Also,
these factors are presumed to be behind the persistent outbreaks in other countr
ies, such as Cambodia and Laos. In Thailand, for instance, the proportion of you
ng ducks in flocks was found to peak in September–October; these rapidly growing y
oung ducks can thus benefit from the peak of the rice harvest in November–December
, at the beginning of the cold weather. Thailand, Vietnam, Cambodia and Laos, as
opposed to Indonesia, are located in the northern hemisphere. This peak in the
congregation of ducks in November–December indicates the period in which there is
an increase in the chances of virus release and exposure, where rice paddies oft
en become a temporary habitat for wild-bird species. The influenza season in hum
ans begins close to this peak.

Conclusions
In temperate climates, the strict dependence of influenza infection on environme
ntal temperature makes it improbable that the primary human-to-human transmissio
n of influenza is through warm biotic droplet infection. Influenza must be trigg
ered by an abiotic vehicle that is increasingly efficient in spreading infection
with increasing cold environmental temperatures. Therefore, the question arises
as to which abiotic vehicles are dependent on cold environmental temperatures f
or the transmission of influenza viruses. Drinking water is such an abiotic vehi
cle.
This article shows that cold drinking water may be the abiotic vehicle by which
virulent human influenza viruses from the infection reservoirs reach humans, and
which is responsible predominantly for triggering the seasonal influenza epidem
ics. This also applies specifically to the new H1N1 influenza virus with vomitin
g or/and diarrhoea (38% of cases) and the lethal H5N1 avian influenza virus, who
se potential transmission via water is well established.

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Dipl.-Ing. Wilfried Soddemann


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D - 48351 Everswinkel
soddemann-aachen@t-online.de
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