Prion Disease Transmission

By McDonnell, Gerald

KEYWORDS Decontamination / Inactivation / Prion / Sterilisation Prion diseases present unique challenges to healthcare facilities, both in the care and treatment of patients. A significant cause for concern is in the routine reprocessing of medical devices used on patients and how disease transmission can be prevented on the reuse of devices. Investigations have shown that prion disease can be transmitted on medical devices, which can be a concern given the long incubation times associated with these diseases and that guidelines to control transmission only really apply in a small number of known or at risk cases. It is only recently that medical device-associated cleaning, disinfection and sterilization technologies have been investigated and the results of these studies are summarized in this report. The evidence would suggest that many simple decontamination steps can be applied to dramatically reduce the risks to patients, but the research has also given some surprises. Overall, it is reasonable to expect that standard precautions will be able to be applied both today as well as in the future to reduce the risk of prion disease transmission as well as the many other human pathogen concerns, although this may mean changes in some of our practices.

Introduction

Microbiology is truly a developing science. Although our understanding of the microbial world has increased dramatically over the last 150 years, we continue to identify and understand new types or micro-organisms and challenges in their control. Examples include ‘new’ (or to be correct, newly-identified) types of protozoa, viruses, bacteria (for example, antibioticand biocide-resistant strains) and nonconventional agents. Infection control and prevention practices need to be constantly challenged to ensure that we are truly achieving the goal of reducing the risks associated with the presence of microorganisms, particular pathogens, and preventing their iatrogenic transmission to patients and staff.

Many readers will remember a significant debate some 20 years ago on the identification of Human Immunodeficiency Virus (HIV) as the viral pathogen responsible for Acquired lmmuncDeficiency Syndrome (AIDS) and initial speculation on the efficacy and safety of various standard disinfection and sterilisation techniques (Conte 1986). How would patients be cared for, and during surgery/device reprocessing would decontamination procedures be effective to remove/inactivate the virus?

Today it is widely-accepted that HIV, from a disinfection point of view being classified as an enveloped virus, is actually relatively susceptible to heat and a wide range of chemical biocides and products (see Figure 1). In the meantime, a further challenging threat to human health has been identified. These agents, known as prions, are associated with rare but severe diseases that are always terminal in patients once identified; they are infectious, have been shown to be transmissible on surgical instruments and are widely referenced as being extremely resistant to decontamination methods (Baron et al 2001, McDonnell 2007). This paper will briefly review the challenges associated with these unusual diseases, with a particular emphasis on the risks of iatrogenic transmission in perioperative practice.

Prions and associated diseases

Prion diseases, otherwise known as transmissible spongiform encephalopathies (TSEs), are fatal degenerative brain diseases. Notable examples include Creutzfeld-Jacob disease (CJD), variant CJD (vCJD) and Bovine Spongiform Encephalopathy (BSE). Current epidemiological evidence suggests that prion diseases in humans are actually very rare.

‘Sporadic’ Creutzfeldt-Jakob Disease (CJD) is the most prevalent, with an average rate of at least 1.1 in a million population worldwide, although a rate of as high as 2.34 in a million has been reported in Austria and Switzerland since 2001 (presumably due to more active surveillance/diagnosis). These transmissible diseases are unusual in that they are proposed to be caused by protein, and specifically the conversion of normal human PrP protein into an abnormal PrP (PrPres) form (Baron et al 2001). The conformational change of the normal protein structure renders it unusually resistant to normal cellular degradative processes, leading to accumulation and cell damage, with particular consequences to neural tissues. This is indeed a difficult concept for many microbiologists and infection control personnel as unlike other infectious agents such as bacteria and viruses, these proteins are not associated with any known nucleic acids, although the true nature of the infectious agent remains under investigation. Further, there are other human diseases that are similarly linked to protein accumulation and deposition including Alzheimer’s and Parkinson’s disease, although unlike prion diseases these have not been reported to be linked to any transmissible agent (with the recent exception of initial reports on transmission of Alzheimer’s disease in animals (Meyer- Luehmann et al 2006).

Figura 1 Microbia! resistance profiles to disinfectants and sterilants (based on McDonnell & Russell 1999, McDonnell 2007). The profile on the left is widely cited and the basis of disinfection and sterilisation practices. The profile on the right represents the wider spectrum of micro-organisms, with the true resistance of prions under continued debate. In both cases the resistance profile can vary significantly depending on the physical or chemical method applied.

Clinical implications

It has been known for some time that medical devices contaminated with prions can transfer the disease to patients. The first known report was published in 1977 with CJD transmission in two patients as a result of contact with contaminated intracerebral electrodes previously used in the brain of a person with the disease (Bernoulli et al 1977). Although it is important to highlight that the reprocessing methods used in this case may have been suboptimal (using formaldehyde), it was clear from this landmark investigation that CJD could be repeatedly transmitted to multiple cases on which these devices had been used. Further, these devices remained infectious three years after the initial use of the device on a CJD patient! Other studies have revealed at least four other cases of probable iatrogenic transmission that occurred as a consequence of neurosurgical procedures (Weissmann et al 2002). These studies are further supported by experimental evidence that show disease transmission on device surfaces and contaminated tissues (for example, as first shown by Zobeley et al 1999 and subsequently by Van et al 2004 and Pichet et al 2004).

In considering the risks of surgical device contamination and reducing the risks of transmission, little has changed over the years from the Infection Control Guidelines for Transmissible Spongiform Encephalopathies issued by the World Health Organization (WHO) in 2000 including:

* Establishing, documenting and implementing a facility policy (this is particularly important to note as many hospitals in the UK and other countries may still not have put such a policy in place).

* Identifying risk groups (for example, patients with a family history of the disease) and tracking these specific cases. This is achievable but only represents a small proportion of cases, with 80% of CJD cases alone known to be sporadic in nature (therefore associated with no known risk factors) and considering the relatively long period of incubation (years) of these diseases in subjects (Baron et al 2001, Weissman et al 2002).

* For high risk surgical procedures or tissue (such as the brain) contact, to:

consider the use of disposables

consider incineration of the devices

use specific, yet harsh, decontamination procedures, with an emphasis on rigorous cleaning, chemical decontamination (for example, with 1-2N NaOH for 1 hour) and/or elongated steam sterilisation (for example, 134[degrees]C for 18 mins). Many of these methods are, however, considered damaging to devices.

However, since 2000 research has continued into these diseases and especially on the various decontamination procedures that can be used to reduce the risks of surface contamination. Notably these have included (and discussed in further detail in other reviews such as Fichet et al 2007 and Sutton et al 2006):

* The high affinity of the prion protein for surfaces and the difficulty to physically remove them.

* The detection of relatively high levels of protein on medical device surfaces, despite the use of validated cleaning procedures.

* Cleaning with various detergent formulations can increase or decrease the resistance of prions to steam sterilisation.

* The development of new test methods to evaluate the efficacy of surface decontamination methods and procedures.

* The detection of prion proteins in peripheral organs, in particular in vCJD cases with detectable levels in the spleen, tonsils, thymus and appendix.

* With more sensitive assays, the detection of prion proteins in various tissues from CJD cases and models, including muscle tissue and depending on the stage of the disease.

* Demonstrated blood transmission of these diseases.

* The potential of dramatic differences in the resistance of various prion strains to inactivation methods.

* Further debate on the true nature of the disease-associated agent. * The importance of universal precautions, due to the sporadic nature and long incubation periods (which are now known to even be up to 50 years) associated with these diseases.

Recent guidance in the UK

The UK has had a strong and unique interest in prion diseases, in particular on the identification of variant CJD as a disease and the association with the BSE outbreak that had a particularly dramatic impact. Despite this, the specific recommendations on managing the risks associated with iatrogenic transmission on reusable devices are considered minimal in comparison to other countries (Fichet et al 2007). With all the scientific reports and debates listed above it is often difficult to determine what is the true impact to patient safety and perioperative practice. However, a recently released guideline from the National Institute for Health and Clinical Excellence (NICE) entitled Patient Safety and Reduction of Risk of Transmission of Creutzfeldt-Jakob Disease (CJD) via Interventional Procedures (NICE 2006) provides practical, independent advice. This guidance covers the management of all patients undergoing procedures involving instruments and endoscopes that might pose a risk of transmission. The guidance is provided in three parts: the full guidance (IPG196), a Quick Reference Guide (N1148) and a General Guide on Understanding NICE guidance (N1149). The guidance offers a useful update on patient safety, with consideration of published and unpublished data reviewed by the advisory committee to include:

* The guidance continues to advise hospitals and other healthcare facilities to consider the ACDP TSE (Advisory Committee on Dangerous Pathogens Transmissible Spongiform Encephalopathies) Working Group recommendations in cases of known or suspected TSEs (ACDP TSE, 2005). These recommendations outline safe working practices and prevention of infection, including management arrangements for infection control, identifying risks groups, hospital care or patients and surgical procedures/decontamination.

* The guidelines are applied to the general population, with a continued emphasis on the reduction of risks associated with high risk tissues and high risk procedures. These are specifically related to intradural neurosurgical operations on the brain (excluding operations on the spine and peripheral nerves), neuroendoscopy and posterior eye procedures that involve the retina or optic nerve. Of particular note is emphasis on the tracking and traceability of devices, to ensure that instruments remain within designated sets and to prevent mixing of devices between sets.

* For neuroendoscopy, rigid devices (that can be steam sterilised) are preferred and all accessories should be single use.

* Separate sets of new neuroendoscopes and reusable surgical instruments for use in high risk procedures are recommended for use only with children born since 1 January 1997.

* Single use instruments are not generally recommended, apart from certain accessories (For example, as described for neuroendoscopy) but if they are used they should be of the same quality as reusable devices.

* The guidance expects that new methods of removing prions from medical devices will become more widely available within the next five years. For this reason, the guidance will be reviewed within two years of release.

These guidelines have however been controversial. This has included the practical implementation of the recommendations in hospitals and need for further research on the impact of the drying of soil on devices and on the use of new decontamination procedures. For this purpose, the Engineering and Scientific Advisory Committee- Prions (ESAC-Pr) has been formed as a cross-functional group to formally review and Implement new decontamination technologies/ practices across the NHS (McDonnell & Tomlinson 2007). This group will work closely with the existing Spongiform Encephalopathy Advisory Committee (SEAC) that provides independent scientific advice specifically on these diseases.

Overall, these guidelines highlight the importance of a coordinated effort by the hospital, with particular emphasis on a close working relationship between the operating room, treatment centres and sterile service departments.

Issues in instrument transport and drying

One area of particular concern is the impact of drying of soil on the surface of devices, with the NICE guidelines specifically recommending further research into the practice of keeping instruments wet during transport/storage and prior to reprocessing (NICE 2006). This issue is not new and the current ACDP recommendations on device reprocessing already recommend that instruments should be kept moist and cleaned as soon as possible following clinical use (ACDP 2005). In fact, this requirement is not widely practiced in the UK but is indeed standard practice in other countries, including the US (AAMI 2003).

Overall, it is known that prion-related infectivity is more tightly bound when allowed to dry on a surface and, as they are hydrophobic (‘water-hating’) proteins, are difficult to remove by simple washing. It is also generally well known that patient soils are much easier to clean when they are not allowed to dry. There are a wide range of methods and products used for the safe transport of, and prevention of drying on, devices from the site of patient use to a reprocessing area. These include various pre-soaks, gels, foams, enzyme detergents and coverings. The benefits of these include drying prevention, instrument protection (noting that dried soil is one of the leading causes of damage, in particular rusting, on reusable devices), optimised cleaning efficiency, worker protection and infection control.

However, users should also be aware of concerns with instrument transport products (depending on the product type), including not being able to see sharp instruments under foams, bacterial multiplication (if not adequately inhibited), and not adding other safety risks. Of key importance is that these products can only practically be applied in the operating room and directly following surgical use. This has an important advantage to perioperative practice, in that for some years many operating theatre staff have become distant from playing a role in the decontamination cycle. This may need to be reinvestigated, in particular to allow for closer working relationships between the perioperative and decontamination departments with the singular goal of instrument and patient safety.

Issues in cleaning

Rigorous cleaning is often cited as the most important step in device reprocessing to ensure adequate disinfection and/or sterilisation, but also in reducing the risk of prion contamination. Cleaning can include multiple steps such as manual, semimanual (for example, in an ultrasonic bath) and automated in washerdisinfectors. Various guidelines and standards (for example, in the UK the new HTMOl-Ol guidelines and the newer ISO EN BS 15883 washer disinfector standards) have dramatically improved the reliability and performance of washerdisinfectors, although the machine is only as good as the cleaning/disinfection/ drying process used and validated.

An important consideration is the cleaning chemistry (or ‘detergent’) used. Cleaning chemistry formulations include a variety of actives (for example, enzymes, acid, alkaline and surfactants) and inert ingredients that combine to give the overall desired attributes of the detergent: optimal activity, standard activity in good or bad water quality, an adequate shelf life and to protect devices from damage. The various effects of these formulations on prions have only recently been tested, with some surprising results. For example, some enzymatic cleaners have been shown to decrease the risk of prion contamination by efficient removal from contaminated surfaces, while other enzymatic cleaners have the opposite effect by increasing the resistance of the infectious agent to subsequent steam sterilisation (Pichet et al 2004, Van et al 2004).

This could be considered an issue with all cleaning chemistries and not just enzymatics. Consider any chemical that is used in the operating room and sterile services department on a medical device (for example, iodine). The most effective cleaners to date have been shown to be alkaline detergents, as these chemistries are particularly good at removing and even breaking down proteins from surfaces. An example is HamolOOPID, which is CE marked to reduce the risk of surface prion contamination (Figure 2).

It is important to note that alkaline chemistries will vary dramatically depending on the pH, alkalinity, formulation effects, contact time, concentration, temperature and compatibility with device materials. It is strongly recommended that before using a given chemistry that users should obtain data to substantiate any claims in writing from detergent manufacturers. In the UK, for example it is recommended that data should be provided against multiple strains of prions, including a vCJD, due to concerns over strain resistance profiles.

In the future it is clear that a greater number of detergent formulations will be made available to health services, based on many recent reports, publications and patents (as reviewed by Fichet et al 2007). These include:

* The use of specific proteolytic enzymes (proteases), in particular under alkaline conditions, that have been shown to break- down the prion protein and reduce infectivity (for example, enzymes such as ‘Prionzyme’ and the class known as keratinases, under specific conditions).

* The combination of various ingredients in detergent formulations to give prion inactivation (for example, acidic detergent mixtures and various enzyme-based formulations in combination with specific ingredients).

* Further alkaline formulations that are under test.

* Advanced cleaning methodologies including plasma cleaning technologies cited by a number of investigators. It is clear that many of these technologies will be available over time and will show successful application in device reprocessing.

Issues in disinfection/sterilisation

Prions are often cited as being ‘resistant’ to heat, but this statement should be put into perspective: prions have an increased resistance or tolerance to heat in comparison to many other pathogens (disease-causing agents) and further testing is required to show what the impact of heat-based methods are as they are used in healthcare facilities.

For example, many of the test methods used before to evaluate steam sterilisation involved placing grossly contaminated surfaces with prion-infected brain homogenates directly into a steam process. It is clear that this does (or should) not reflect clinical practice, as direct treatment with steam in these cases can lead to clumping of extraneous material and protection from the steam. A better investigation would be to test the impact of typical reprocessing cycles, including cleaning, disinfection and sterilisation in steam. Some of these experiments are actually underway at various locations at the time of writing this article. First, the impact of cleaning needs to be understood and, as discussed above with emphasis on the cleaning chemistry, can both increase or decrease prion resistance to subsequent processing. second, what is the impact of heat disinfection? This is certainly a different process to steam as the material is maintained hydrated (i.e. in water), is first heated to the desired disinfection temperature and then held for the disinfection time. Let us not take for granted that by increasing the temperature that we get better results, as we expect for micro-organisms like bacteria and viruses. Some experiments have shown that boiling or heating in water can dramatically reduce the infectious titre of prions (including multiple strains of prions – as discussed by Taylor 2001 and Fichet et al 2004). This may be further increased in combination with certain chemistries, such as surfactants and chelating agents. The overall impact of the cleaning/heat disinfection process is clearly an area of further research and may, under the right conditions, be adequate to reduce the risks of prion infectivity to safe levels prior to further reprocessing.

Steam sterilisation itself is an effective process against prions, although the data and conclusions in the literature vary considerably. It seems more than possible that these variable results are due to technique issues and the respective test methods used. Many of these tests were performed on liquid suspensions of brain preparations, which is often not representative of surface contamination during steam sterilisation. Further, with the gross- contamination loads used in these tests, it has always been shown that steam sterilisation (under temperatures typically ranging from 121[degrees]C to 138[degrees]C, and exposures times varying from three minutes to one hour) dramatically reduces the levels of prion infectivity.

There have been some interesting findings in many of these reports including increased resistance depending on pretreatment prior to testing, increased efficacy of steam when testing was performed under hydrated conditions (i.e. contaminated surfaces suspended in water) and an indication of greater resistance to higher steam exposure temperatures. One consideration is in the manner of exposure, where it is known that when gross soil is directly exposed to steam (for example, in a vacuum-based steam sterilisation process) that this will cause soil clumping and possible prion protection from heat penetration, in contrast to more initial gentle heating of the material under liquid conditions (which will cause protein unfolding and soil penetration) and then raising the temperature over time (to cause protein fragmentation and loss of function). Clearly we have more to learn about the impact of heat and steam sterilisation on optimal prion inactivation.

It is also clear that many chemical disinfection and sterilisation processes may dramatically reduce prion contamination on a surface. In past studies, these chemicals were tested alone and not in formulation (when mixed with other ingredients) or under process (for example, temperature, gas or liquid, humidity, and so on) control, as they are actually used in clinical practice (McDonnell & Burke 2003). The choice of chemical type is an important, initial consideration. Any chemical with the primary mechanism of action of protein cross-linking or coagulation may not be desired, as is the case for aldehydes (such as glutaraldehyde, formaldehyde and OPA), alcohols and phenolics. Although, it is interesting to note that one phenolic-based general surface disinfectant has been confirmed as effective by a yet unknown mechanism of action (Race & Raymond 2004).

Other chemicals that are recognised to break down proteins under certain conditions are more likely candidates for further investigation. Particular emphasis has been placed on oxidising agents, including the halogens (for example, sodium hypochlorite, as a source of chlorine, is already widely used for general surface disinfection with prion contamination, although at high concentrations and long exposure times) and peroxygens/other forms of oxygen (for example, hydrogen peroxide, ozone and peracetic acid). Peracetic acid was particularly highlighted for endoscope decontamination purposes, although only one formulation with this chemical has actually been shown to be effective tp reduce the risk of prion contamination (Antloga et al 2000, Pichet et al 2004). It is now known that this effect is based on the combination of ingredients in the formulation with peracetic acid and dependant on the temperature (with protein breakdown shown at >45[degrees]C). It has also been shown that other peracetic acid-contaminating products may have the opposite effects showing surface fixation, highlighting the importance of specific formulation (rather than the actual antimicrobial chemical) evaluation (Kampf et al 2004).

Figure 2 Examples of two products that have been verified to significantly reduce the risk of prion contamination, as verified against multiple strains of prions. The product on the left is an alkaline cleaning detergent for routine cleaning (manual or automated) and on the right is a new hydrogen peroxide gas based system (the V-Pro1).

Further investigations are warranted with these ingredients to optimise the activity of peracetic acid and other liquid oxidising agents against prions. Interesting results have also been shown with gaseousbased oxidising agents, in particular hydrogen peroxide, ozone and various gas plasmas. In the case of gaseous hydrogen peroxide, dramatic reduction in prion infectivity has been confirmed under atmospheric and vacuum conditions, although it is important to ensure that liquid (or condensed) hydrogen peroxide is not formed during the gas process as this appears to cause material clumping and little activity in comparison to the gas (Fichet et al 2004, Van et al 2004, Pichet et al 2007).

A new low temperature sterilisation process based on hydrogen peroxide gas has already been made available, which includes verified efficacy against multiple prion strains (Fichet et al 2007, see Figure 2). Initial reports on the effectiveness of ozone are under further investigation, while gas plasmas (including nitrogen, hydrogen peroxide and oxygen plasmas) are of particular interest as various oxidising agents (including hydroxyl radicals) are formed during the plasma-generation process that may have similar inactivating effects (Baxter et al 2005).

Overall there is much scope for investigations into both high and low temperature disinfection and sterilisation processes to be effective against prions, although as in the case of cleaning chemistries the detail on how these are applied and controlled may have a significant impact on their effectiveness.

Perspectives for today and the future

It is certainly true over the last five years that our understanding of the science of prions and specifically prion decontamination has come a long way. The first step has been the greater emphasis placed on successful and validated cleaning of surgical devices, with the various guidelines and standards playing an important role to update reprocessing departments. These practices are now rolling into other areas, including dental practices and out-patient facilities.

These advances are clearly not only important for reducing the risks of prion contamination, but have a much wider implication in the safe reuse of surgical and investigatory instruments. Cleaning chemistries are available, and will be further developed, that are known to efficiently remove and inactivate prions. In addition, initial trials with some of these chemistries have suggested that more efficient (even microscopic) cleaning of device surfaces are achievable, with decreased rejections of devices on inspection following automated cleaning/disinfection.

A step that has been highlighted, even prior to cleaning, is the prevention of devices from drying following surgical use and during transport to the sterile services department. This already makes scientific and practical sense, with the added potential benefits of reducing device damage and improving cleaning when applied correctly. Investigations will continue into heat disinfection and sterilisation methods, but it is already known that some of these processes are already efficient at prion inactivation. Some existing and developing chemical, low temperature disinfection and sterilisation methods are also showing effective prion inactivation, which all but closes the loop in the needs for reprocessing cycles.

Overall, it is now possible that the whole reprocessing cycle will be adequate to reduce if not completely remove any risks of prion cross-contamination. However, as highlighted in the literature, the overall process should be tested to ensure that certain steps in the process (for example, soil drying, chemical or heat clumping, and so on) do not significantly have negative effects on the required outcome. Finally, it seems more than likely that in the near future prion decontamination will be an existing component to standard precautions during device reprocessing and perioperative handling of devices, just like any other disease-causing agent. This is practical but not without challenges and changes to our current practices and perceptions.

Conflict of interests

This article expresses the opinions of the author alone, based on a review of the literature, and in no way represents the views of his employer.

Provenance and Peer review: Commissioned by the editor; Peer reviewed.

The evidence would suggest that many simple decontamination steps can be applied to dramatically reduce the risks to patients

There should be an emphasis on a dose working relationship between the operating room, treatment centres and sterile service departments

There is much scope for investigations into both high and low temperature disinfection and sterilisation processes

References

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Dr Gerald McDonnell

Correspondence address: STERIS Limited, Jay’s Close, Viables, Baslngstoke, Hampshire, RG22 4AX. Email: gerry_mcdonnell@steris.com

About the author

Dr GeraM McOonnetl BSc, PhD

Vice President, Research and European Affairs, STERIS Ltd, Baslngstoke

Copyright Association for Perioperative Practice Jul 2008

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