Unwelcome colonisers: biofilm formation on voice prostheses

A human being’s voice is one of their most distinguishing and individual features. Most of us have experienced the frustration of temporarily losing our voices – but for many survivors of laryngeal cancer (cancer of the voice box), this loss is permanent. A laryngectomy, or full removal of the larynx, is a common last resort to treat this cancer if other options have failed. This operation disconnects the windpipe from the nose and mouth, leaving the patient to breathe through a hole in their neck called a stoma. The side effect of this operation, however, is that patients lose the ability to speak.

The challenge of giving these patients a voice has been partially solved; voice prostheses (VP) have been developed to allow people without larynges to speak again, albeit on a severely limited scale. A VP is a one-way valve that is placed into a puncture between esophagus and windpipe. If the stoma is covered, this valve allows air to escape through the esophagus and the mouth. With considerable training, people can then use this air to produce sounds in a variety of manners. An example of voice prosthesis speech can be heard in this video.

Voice prostheses are not without their problems. Biofilms – a sticky mass of microbes – clog the prostheses’ valve, preventing it from fully opening or closing. Saliva, microbes and other particles can leak into the windpipe and the trachea, where they can cause infections and dangerous diseases such as aspiration pneumonia. Candida albicans, one of the most common species of yeast in VP biofilms, is also capable of penetrating into the silicone of the device, eventually rendering it completely unusable. Together, these issues mean that VP lifespan is shortened dramatically – in some patients, prostheses may only last a few weeks. Most patients then require further valve replacement surgery.  The picture below shows a valve only three months after insertion.

A team of researchers, led by Dr Campbell Gourlay, a molecular cell biologist at the University of Kent, and Professor Fritz Mühlschlegel, a Consultant Microbiologist at East Kent University Hospital Trust, are working to understand how best to stop the formation of biofilms on voice prostheses. Dr Gourlay explains that these biofilms are formed by organisms that live naturally in our mouth. These microbes pose no threat to us as long as our immune system functions properly and keeps them in check. However, the chemotherapy that patients receive to treat their cancer tends to leave them severely immunocompromised. Under these conditions, microbes can grow and multiply rapidly on the voice prostheses, forming biofilms where they might not be able to in a healthy individual.

It is not completely understood why voice prostheses – and other artificial objects in patients’ bodies, such as catheters – are such attractive places for biofilms to form. One contributing factor is that the surfaces of such devices are generally made of silicone, a material with excellent mechanical properties that is easily molded and that looks very smooth to our eyes. However, high-resolution microscopy conducted by Dr Gourlay’s group reveals that at the microbial scale, silicone surfaces look more like mountain ranges, with numerous peaks and valleys for microbes to attach to.

Recent studies have shown that there are other exacerbating factors. For example, C. albicans becomes better able to colonise surfaces in CO₂-rich environments, such as those provided by exhaled breath. Furthermore, environments that experience shaking and friction are more easily colonised by biofilms than calmer areas. This seems counterintuitive at first, but such stresses cause microbes to release adhesive proteins in greater number to better enable them to cling to surfaces.

In a recent review in the Journal of Medical Microbiology, Dr Gourlay and his colleagues review some recent avenues of research. Among others, researchers are looking into surface coatings that could delay the onset and growth of biofilms. Metals such as palladium, titanium or even gold are being used, but it has not been conclusively shown that these coatings significantly reduce biofilm formation. Other options include coatings made from compounds with disinfectant or hydrophobic properties. So far, such methods are simply not cost-effective as they multiply the cost of a prosthesis but, on average, only extend its lifetime by a few weeks. Dr Gourlay suggests that ceramics may be of the more promising materials: they are smoother than silicone, extremely durable and less expensive than rare metal coatings.

Fortunately, there are far simpler ways in which VP users themselves can extend the lifetime of their device. A study has shown that prostheses in India tend to last much longer than in other countries. One possible explanation for this finding is that buttermilk, which is slightly acidic and has potential anti-microbial properties, may be an example of the strong influence that diet can have upon biofilm formation. Further research into the diet of laryngectomy patients and its impact on VP longevity will reveal whether the old adage ‘we are what we eat’ can be applied in this case.

The research Dr Gourlay and his team undertake is likely to have beneficial spillover effects for other indwelling surgical devices. A major research and development centre for VP devices has also recently been established. Along with simple nutritional changes that prolong prosthesis lifetime, the future of their users is hopefully set to become brighter, easier and more comfortable.