Prions in Biosolids

Anaerobic digestion inactivates prions.

That was the bottom line to Greg Kester’s email to us this past week. You can all let out a great sigh of relief. Knowing this, you can now handle the most recent “prion scare.”

What is a prion?  Like the term “biosolids,” prion is an invented word. It was derived in 1982 for a new “biological principle of infection” reported in Science by Stanley B. Prusiner, in the paper “Novel proteinaceous infectious particles cause scrapie”, research for which he received the Nobel Prize in Medicine in 1997.

What is prion disease?  According to several journal sources, prion disease, also known as ”transmissible spongiform encephalopathies,” or TSE is an invariably fatal, neurodegenerative disorder affecting humans and animals, in which aggregations of PrPSc, an abnormally folded prion protein, accumulates in affected tissues and induces conversion of normal protein. Infective prions have been shown to be transmitted orally, to arise spontaneously in the brain, or to derive from gene mutation.  Prions underlie such diseases as Creutzfeldt-Jakob disease, bovine spongiform encephalopathy and scrapie.  So, yes, prion disease sounds scary.

What is the scare for the biosolids professional?

Kester from California Association of Sewerage Agencies, reported that a blogger posted “Neurological Disease Becoming The Leading Cause Of Death.”  The blog was basically a rant against biosolids recycling:  “… we are recycling the pathogen that causes Alzheimer’s right back into our food and water. We’re dumping these killer proteins on crops, parks, golf courses, ski areas and school grounds. Rain and irrigation spread them throughout our communities and watersheds. We’re dumping prions into our food and water supplies with foolish sewage management practices.”

Kester wanted to remind the biosolids profession of the sound science behind its claim that prions are not an issue in biosolids. WEF has on its website a good Prion Fact Sheet describing the issue.  Importantly, Drs. Ian Pepper and Chuck Gerba, environmental microbiologists at the University of Arizona long engaged in researching microbial exposures to biosolids, have studied prions. Their 2011 journal study report, “Survival of infectious prions in Class B biosolids,” led to the WEF 2014 information sheet Kester distributed last week, Survival of Infectious Prions during Wastewater Treatment. Pepper and Gerba made reference to an earlier 2001 journal article by Gale and Stanfield in “Towards a quantitative risk assessment for BSE in sewage sludge.”  And, they advanced the case for biosolids by developing a lab method for distinguishing active from inactive prions in environmental samples and applying it to digested biosolids samples.

Even knowing we have this solid foundation for confidence in the safety of biosolids, the blogger’s rant left me feeling disconcerted. I had not heard Alzheimer’s Disease being implicated with prions, or with biosolids for that matter, and no one had asserted a connection between biosolids and the two prion diseases which have affected people: Creutzfeldt-Jacob Disease (CJD) and Bovine Spongiform Encephalopathy (BSE).

I started out with the Creutzfeldt-Jakob Disease Fact Sheet from the National Institutes of Health. Here you can learn that “CJD” is one of several “prion diseases.” That fact sheet explains that prions are implicated in several other exotic diseases. In humans, cannibal traditions of the Kuru leads to brain wasting.  Scrapie is the prion-mediated disease in sheep that Dr, Prusiner had studied, and among deer-related wild animals in northern United States Chronic Waste Disease is prevalent.

CJD is a rare disease, with only 300 new cases annually.  It seems to arise without known cause in the brain, or through a gene defect. With CJD there is no evidence of transmission through casual contact among family members or with caregivers, which argues against a hazard of typical water and air mechanisms.  Only about 1% seem to be from direct exposures, as to brain material from infected animals, through consuming a diseased animal or through use of a contaminated medical device.

BSE is the infamous media-coined “Mad Cow Disease.”  Its genesis is a real health scare, first identified as a disease in cattle in 1986 and leading to significant cattle mortality (over 100,000) in 1993. The first human death attributed to eating diseased meat occurred in 1996, and the current count as of 9/2014 is 177. One up-to-date source on BSE is from CNN: Mad Cow Disease Fast Facts. While the story has some tragic and worrisome dimensions, the bottom line is that the disease has been stopped in the UK, and the disease was not spread to the United States.

So how was BSE stopped? No more feeding of “MBM” (Meat and Bone Meal) to cattle, and no “downers” sent into the human food chain. As of January 2015, beef from Ireland is now being imported into the United States, so comfortable now are the health officials with their control over BSE.

On the face of it, prions don’t seem a big deal.  The human prion disease CJD is scarce and is not transmissive. The livestock version, BSE, is under control and is carefully guarded. The wildlife version, Chronic Wasting Disease, doesn’t jump to humans or cattle.  So why the concern?

Prion is the perfect metaphor for a deadly horror--an , lying in wait, uncurable. Prions touch upon a primeval human fear. This point was well made in “Biosolids Hits The Fan,” an essay presented at the WEF specialty conference in 1998 by Pulitzer-Prize-Winning science writer Jon Franklin, reminding us that our society does not trust science. While the immediate concern for BSE burned itself out some 15 years ago, the BSE scare provides lessons to scientists, public health officials and the media on risk communication.  The prion controversy has also sparked its own popularized non-fiction book by Jay Ingram -- Fatal Flaws: How a Misfolded Protein Baffled Scientists and Changed the Way We Look at the Brain.

The blogger’s rant touched on Alzheimer’s.  Indeed, recent research has gone into understanding “prion aggregation” and “protein folding” as phenomenon in common with such major diseases as Alzheimer’s Disease (5 million US citizens), Multiple Sclerosis (300,000 US citizens), Amyotrophic Lateral Sclerosis, or ALS (30,000 citizens), and even Type 2 Diabetes. They each may have a genesis in “amyloid folding” of a protein in a way that makes it self-replicating.  If that is the case, then prions go from being implicated in a nearly vanishingly small number of human cases to instead being a factor in the diseases of many millions in the US.

Prions are highly resistant to decomposition. They are not readily decomposed by microbial action.  Reported by Pederson, in Microbial and enzymatic inactivation of prions in soil environments: “Prions are remarkably resistant to inactivation and can persist and remain infectious in the environment for years.”

The use of common sterilization techniques of steam, alcohol, and UV light are not effective methods of sterilization.  This is a particularly acute issue, not for wastewater managers, but for the healthcare industry. One reason is that some of the early and tragic cases of prion-disease transmission occurred inadvertently during normal hospital procedures through iatrogenic means, in other words, via contaminated diagnostic equipment. A second major reason is that many new pharmaceutical products are “biologicals,” meaning they are manufactured from living organisms, and another inadvertent means of transmission is using bovine-derived surgical grafts containing prions; this, too, has happened. This is all well summarized in the National Institutes of Health CJD report.

My unease with the prion issue emerges also from journal articles over the past year on environmental pathways of prion transmission.

The first issue is that soil is a reservoir for prions.  The research into this was directed toward understanding the pathways for transmission of the Chronic Wasting Disease that affects deer in northern U.S.  Soil-mediated prion transmission: Is local soil-type a key determinant of prion disease incidence? , a 2014 article from researchers in Nebraska, concluded “soil could serve as an environmental reservoir of prions, facilitating disease transmission.” Fine textured soils, rich in organic matter, worked best at retaining prions. The article “Pathogenic prion protein is degraded by a manganese oxide mineral found in soils” made the observation that soil effectively holds prions close to the soil surface, close to grazing animals.

The second issue is plant uptake of prions. Methods developed by prion researcher Claudio Soto allows for quantification of prions to the very low concentrations shown to be infective. When this method was applied to the question of plant uptake, the finding, reported in his article “Grass Plants Bind, Retain, Uptake, and Transport Infectious Prions,”  was that: “plants can uptake prions from contaminated soil and transport them to aerial parts of the plant (stem and leaves).”

The circle is complete. Prions from diseased animal are discharged through excreta, harbored in the soil, taken up by plants, and finally consumed by othe animals. These articles thereby advance the understanding of how prion disease may transmit “horizontally” across the landscape of animal populations. They further serve to explain the anxiety of those concerned with biosolids land application, or for any and all manures or wild animal populations, for that matter.

What does this all mean for the biosolids professional? What I recommend is that our wastewater treatment and biosolids processing technologies be evaluated for their effectiveness as barriers to transmission of infective prion proteins. Drs. Pepper and Gerba have given us a tool that can be used for this evaluation.  We need the protocols to follow and the money to apply them.

Prions are not going away, nor can we hide from the health concerns they raise, but we can get on with our part of the science and NOT WASTE OUR BRAINS.