Tuesday, August 13, 2019

Nature: Airborne Transmission May Have Played A Role In Spread Of U.S. 2015 HPAI Epizootic

2015 Avian Flu Epizootic


Over the summer of 2015 - in the wake of the HPAI H5 epizootic that spread across half of the United States and parts of Canada the previous spring - APHIS released a pair of postmortem reports (see APHIS: Partial Epidemiology Report On HPAI H5 In The US and APHIS Releases Updated HPAI Epidemiology Report).
Both studies cited a number of plausible factors that might have led to the rapid spread of the HPAI virus between farms, included movement of poultry, poultry products, equipment and personnel between farms and even raised the possibility that prevailing winds may have carried contaminated dust particles from farm to farm.
While the HPAI H5 virus appears to have been introduced to North America via migratory birds, its subsequent rapid spread eastward - particularly across the American Midwest - appeared unrelated to migratory birds.
 Neither report was able to nail down any `specific pathway or pathways for the current spread of the virus’. 
One theory that has gained traction in recent years is the airborne spread of the virus - carried not by birds - but by minute dust particles. The sort of contaminated particulates that would be ejected in copious amounts from infected poultry barns by their ventilation systems.
The science of all of this even has a name; aerobiology the study of how bacteria, fungal spores, pollen and even viruses can be passively transported in the air.
While long distance transmission of viable flu viruses remains highly  controversial, it isn't exactly a new idea.
  • A little over ten years ago, in The Virus My Friend, Is Blowin' In The Wind, I wrote (albeit skeptically) about claims by Indian officials that their bird flu epidemic was `brought in by winds blowing from Bangladesh'.
  • In 2010 (see Viruses Blowin’ In The Wind?) we saw a report in the journal Environmental Health Perspectives, that suggested that it was possible for H5N1 (or any Influenza A virus) to be transported across long (hundreds of kilometers) distances in the air, although viability was unknown. 
On a much smaller scale, we've seen numerous instances where the `dust’ (desiccated chicken manure, feathers, etc.) from chicken farms or live markets  has been strongly suspected as having spread bird flu – at least for distances of a few hundred yards.
For some human bird flu cases in Indonesia and China, the only known exposure has been listed as living near, or simply walking past, a poultry farm or live market. 
In April of 2015 the idea of farm-to-farm spread via infected dust was openly discussed (see Bird Flu’s Airborne `Division’) by the USDA's  Chief Veterinarian, John Clifford.
(Note: Audio link no longer appears live
The following month (May, 2015), in CIDRAP: H5N2 Roundup & Detection In Environmental Air Samples, we looked at air sampling conducted by the University of Minnesota around infected poultry farms that found evidence of airborne virus particles.
Whether, and for how long (or far), these airborne virus particles remain viable, infectious, and present a minimum infectious dose (MID) is the $64 question.
While it doesn't settle the matter, today Nature.com's Scientific Reports has published a study that presents evidence that long-distance airborne transmission may have been a factor in the spread of avian flu among Iowa's farms in the spring of 2015. 
This is a lengthy, detailed, and often technical report - and while some will find it tough sledding - is well worth reading in its entirety. 
When you return I'll have short postscript.

Airborne transmission may have played a role in the spread of 2015 highly pathogenic avian influenza outbreaks in the United States 

Yang Zhao, Brad Richardson, Eugene Takle, Lilong Chai, David Schmitt & Hongwei Xin

The unprecedented 2015 outbreaks of highly pathogenic avian influenza (HPAI) H5N2 in the U.S. devastated its poultry industry and resulted in over $3 billion economic impacts. Today HPAI continues eroding poultry operations and disrupting animal protein supply chains around the world. Anecdotal evidence in 2015 suggested that in some cases the AI virus was aerially introduced into poultry houses, as abnormal bird mortality started near air inlets of the infected houses.
This study modeled air movement trajectories and virus concentrations that were used to assess the probability or risk of airborne transmission for the 77 HPAI cases in Iowa. The results show that majority of the positive cases in Iowa might have received airborne virus, carried by fine particulate matter, from infected farms within the state (i.e., intrastate) and infected farms from the neighboring states (i.e., interstate).
The modeled airborne virus concentrations at the Iowa recipient sites never exceeded the minimal infective doses for poultry; however, the continuous exposure might have increased airborne infection risks. In the worst-case scenario (i.e., maximum virus shedding rate, highest emission rate, and longest half-life), 33 Iowa cases had > 10% (three cases > 50%) infection probability, indicating a medium to high risk of airborne transmission for these cases. Probability of airborne HPAI infection could be affected by farm type, flock size, and distance to previously infected farms; and more importantly, it can be markedly reduced by swift depopulation and inlet air filtration.
The research results provide insights into the risk of airborne transmission of HPAI virus via fine dust particles and the importance of preventative and containment strategies such as air filtration and quick depopulation of infected flocks.


Because the processes of AI airborne transmission – virus shedding, aerosolization, transportation, deposition, and infection – are not fully understood, this study relied on assumptions based on the best available knowledge.
We assumed that all virus was only shed through feces, although it is also present in poultry’s respiratory tract and thus may be released through respiration51,52. The latter mechanism of AI virus shedding has not been investigated, but some research on other pathogens suggested that the amount may be low53. Virus shedding rate of poultry was assumed constant throughout the infected period; however, this shedding rate could vary at different illness stages. After shed in feces, the virus would not be aerosolized immediately due to the relatively high moisture content of fresh feces54 that prevents fecal particle from becoming airborne.
The ‘latency period’ of aerosolization is an important parameter as it determines the onset of the airborne transmission risk. Studies are lacking that address the latency period directly, although a few reported that this period could be as long as 2 days53,55. The biological decay of airborne AI virus remains investigated. Although AI virus could survive for weeks in water or on surfaces, it may lose infectivity much faster in air, probably due to exposure to adverse changes in humidity, temperature, or radiation56. Virus survival might also vary with different shedding routes.
For example, virus shed through respiratory tract undergoes dehydration stress while virus from feces may undergo both dehydration and rehydration stresses. Information about virus survival responses to the environment stress is lacking. Another vague area is the particle deposition in animal respiratory tract. Depending on the particle size and respiratory mode (nasal vs. oral), the deposition efficiency may vary.

In conclusion, air movement and airborne transmission of HPAI were investigated for 77 Iowa cases of the 2015 outbreak using the HYSPLIT model. During the HPAI outbreak in Iowa, air moved from the infected sites to the recipient sites that were subsequently confirmed positive. The modeled virus concentrations largely depend on the values of the input parameters, such as virus shedding rate, emission rate and half-life.
The estimated virus concentrations did not exceed the MIDs for poultry. The infection probability by airborne transmission was generally low, although 33 Iowa cases were at medium to high risk of airborne transmission under the worst-case scenario. The infection risk seems affected by the house type (open sided vs. fully closed), flock size, and distance to the previously infected farm. The risk of AI airborne transmission may be considerably reduced by inlet air filtration and/or fast depopulation of inflected flocks (e.g., within 24 h).
        (Continue . . . )

The potential long-distance carriage of pathogens on the wind isn't limited to avian flu viruses, as
reported by a 2014 BMC Veterinary Research article  Evidence of infectivity of airborne porcine epidemic diarrhea virus and detection of airborne viral RNA at long distances from infected herds authors Carmen Alonso, Dane P Goede, Robert B Morrison, Peter R Davies, Albert Rovira, Douglas G Marthaler and Montserrat Torremorell wrote:
Results indicated presence of infectious PEDV in the air from experimentally infected pigs and genetic material of PEDV was detected up to 10 miles downwind from naturally infected farms. Airborne transmission should be considered as a potential route for PEDV dissemination.
The following year (2015), in PLoS One: Concentration, Size Distribution, and Infectivity of Airborne Particles Carrying Swine Viruses, some of the same authors returned with a look at the virus carrying capacity of aerosols from experimentally infected pigs.

And finally, in 2018's It's Raining Viruses, we saw a study  from the University of British Colombia, that raised the stakes all the way up to the troposphere - where they found huge numbers of diverse bacteria and viruses - most of which are swept up from the oceans.
Deposition rates of viruses and bacteria above the atmospheric boundary layer
Isabel Reche, Gaetano D’Orta, Natalie Mladenov, Danielle M. Winget & Curtis A. Suttle

All reasons why - despite the current lack of definitive proof - the potential for long-distance spread of virus contaminated particles by the wind needs to be seriously investigated, and mitigation efforts studied and refined.