Fungi have become increasingly significant determinants of human health and may cause as heavy a burden to health as viruses, bacteria and parasites. This outcome has occurred on account of the rise in diseases affecting the immune system and in the risk factors associated with advances in technologies used to treat various diseases and human conditions. These trends are no more evident than in tropical locations. This text emphasizes the biology of fungi impacting human health, with an emphasis on the Asia-Pacific region. The author draws on his own experience working in tropical Australia, Papua New Guinea and Thailand.
A range of information is presented on the natural relationships of fungi, which helps the reader to understand the interactions these microbes engage in with other living organisms including plants and microfauna. Highlighted are the abilities of fungi to survive in soil, on plants and animals and their capacity to adapt to changing conditions and evade attempts to control them. The successes and problems encountered in controlling fungi biologically are outlined, including the development of vaccines. Practical methods to limit the impact of mycotoxins produced by fungi are suggested, including moderating plant growth conditions and being aware of human nutritional status.
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THE BIOLOGY OF fungi IMPACTING HUMAN HEALTHA TROPICAL ASIA-PACIFIC PERSPECTIVE
By WA Shipton
Trafford PublishingCopyright © 2012 WA Shipton
All right reserved.
Microrganisms are capable of causing disease in all categories of living organisms. They include algae, bacteria, fungi, helminths, protozoa and viruses. Among plant populations, fungi and viruses are the most significant disease-causing agents. Among the animal population it is the bacteria and viruses. Fungi, together with algae, helminths and protozoa are eukaryotic in cell organisation, which is quite different to that found in the bacteria (prokaryotes). The viruses on the other hand are non-living agents with no energy generating apparatus.
The fungus kingdom contains an estimated 1.5 million members and may, in fact, be much larger (Hawksworth 2001). Only a small proportion of these are capable of causing disease in animals, but when they do these fungi are often quite difficult to control on account of the similarity in cellular organization and functioning to the host cell.
Fungi have been prominent in previous times in spectacular outbreaks of ergotism (Claviceps purpurea), untimely, mass deaths among turkey poults (Aspergillus flavus), deaths in the human population during times of privation and war through eating contaminated grain (Fusarium species) and during peace as a consequence of predisposing individuals to various forms of carcinoma (Aspergillus species). Then there are the allergic diseases connected with various occupations and the morbidity associated with "sick buildings." The focus on fungi as agents of disease of domestic animals and humans is becoming more pronounced as we enter the age of multiple drug resistance, immunological deficits in individuals due to other diseases and immunological-dampening medications. Then the epidemic of diabetes and fascination with transplant technology has ensured that fungi will be of increasing significance and be challenging in their own right.
While most fungi encountered in the new environments we have mentioned often are present in soils, on plant surfaces and in airspora, they are opportunistic by nature. However, there are also species capable of launching pathogenic attacks in their own right. These continue their significance and in some instances are increasing among specialized groups of people such as diabetics and the immunocompromised. Then there are the zoonotic diseases.
Primary Fungal Pathogens
Primary pathogens are able to cause disease in immunocompetent individuals as well as in the immunocompromised. The portal of entry is commonly via the lungs or it may be through subcutaneous injury. These organisms are encountered most commonly in their endemic areas when aerosolized spores are inhaled following some environmental disturbance (e.g., dust storm, soil cultivation). The organisms encountered here are the dimorphic fungi (possess yeast and hyphal forms) such as Blastomyces, Coccidioides, Histoplasma, and Paracoccidioides (Reiss et al. 2012). The dimorphic fungi are responsible for systemic or superficial infection, which means that spread occurs to organs other than the lungs. The dermatophytes also come into the category of primary pathogens. However, they typically are limited to colonization of keratinized tissues (Hardy 2002). Cryptococcus gattii (Filobasidiella bacillispora) can be considered to be a primary pathogen too. It is typically found among immunocompetent individuals, although immunocompromised individuals commonly are infected. The change in view regarding the status of C. gattii has come particularly following the North America outbreaks of the hypervirulent molecular type VGII. It is able to exist in a range of natural habitats (Bahn et al. 2005, Baddley & Dismukes 2011, Chowdhary et al. 2011).
Diseases of animals and humans may be connected. Among the microbial groups other than fungi, there are well known human disease outbreaks that have commenced in the animal population. These include severe acute respiratory syndrome (SARS) and human immunodeficiency virus/acquired immunodeficiency syndrome (HIV/AIDS), West Nile fever and avian influenza. Previous culprits include Mycobacterium tuberculosis/M. bovis (Baker 2007).
Fungi also are associated with animals and may cross the species barrier to infect human beings. The best known example involves the dermatophytes, those fungi which live on the dermal layers causing diseases of the skin, nails and hair. These are primary pathogens. Microsporum canis is a classic example of a skin disease passing from dogs and cats to human beings. It is capable of passing from stray dogs and causing micro-epidemics in the right circumstances—as has been recorded recently in a day care centre in Brazil (Gürtler et al. 2005). M. canis is common in Southeast Asia too (Lim et al. 1992). Other dermatophytes have the capacity to move across the species barrier (Microsporum and Trichophyton species— Dvorak et al. 2008), although it must not be imagined that all are capable of doing so. Rarely, some largely human-associated dermatophyte infections can move to animals (Dvorak et al. 2008—the so-called anthropophilic group).
The fungi Basidiobolus ranarum, Cyrptococcus neoformans and Penicillium marneffei are associated with animals, but do not fit into the category of zoonoses, except with the possible exception of the latter. For example, Basidiobolus ranarum (syn. B. haptosporus) is carried by kangaroos and wallabies (Speare & Thomas, 1985) besides amphibians and reptiles (Zahari & Shipton 1988, Nelson et al. 2002), but is not associated with disease states in the animals. Specialized geographically defined subgroups of C. neoformans appear to be associated with disease of animals. However, it is not at all certain that cross species movement occurs involving these specialized subgroups (Bui et al. 2008). P. marneffei similarly is problematic. It is capable of causing infection/disease in both humans and selected animal species (Chariyalertsak et al. 1996, Gugnani et al. 2004). The later researchers, working in India, found some evidence, through microsatellite typing, that infection of humans with the animal type was a possibility. However, no genotype was shared by all bamboo rats (Cannomys badius) from all sites.
Opportunistic pathogens are organisms that are able to infect individuals who are compromised in some fashion. They normally do not invade healthy individuals (Reiss et al. 2012). Fungi are found in most habitats including bodies of water. The majority of fungi encountered are able to grow on dead organic matter where they complete their life cycle. In order to survive, the majority of these organisms produce spores and resting bodies that are able to tide them over until a fresh substrate arrives. They commonly are dispersed by rain splash and wind, with assistance from animals, birds, invertebrates and other agencies including humans. Spores are produced often in large numbers and when these are wind dispersed they are widely available. The airspora encountered in the outside environment differs from that indoors, but common elements exist and large numbers of fungal propagules may be available. Some propagules originate from growth on substrates in the building itself (Gregory 1973, Ingold & Hudson 1993, Andersen et al. 2011).
The spores commonly are carried by air currents and lodge on substrates using a number of strategies or are inhaled. If the exposed surfaces contain nutrients and the abiotic conditions are suitable, particularly if moisture and temperature regimes are favourable, then spores germinate and colonization may occur. If the spores are deposited on wound tissues for example, then these unprotected surfaces may be colonized, as in burn victims. Similarly, if the surface of the skin is punctured, the wound may be contaminated by soil and debris and carry with it active hyphae or dormant spores or other survival structures. Fungal spores or vegetative cells may arrive at the suitable site via human activity, as on the hands of surgeons and nurses, surgical equipment, and such like or may originate from the patient's own body. Inhaled spores may give rise to infection under suitable predisposing conditions, such as metabolic acidosis, diabetes, leukopenia (low white blood cell count) and hyperglycemia (Romani 2002, Reiss et al. 2012).
A number of fungi are carried on or in the human body as harmless organisms, such as Candida albicans. If the biological balance existing between these organisms and the multitude of other microbes is upset, such as by antibiotic treatments, illness, pregnancy and other events, the organism may be able to increase its population levels dramatically and cause disease (Timoney et al. 1988, Reiss et al. 2012).
The number of fungi associated with diseases in humans is increasing. There are some limits to the numbers that might be involved as systemic pathogens for they must be able to grow at 37°C. However, the involvement of opportunistic fungi associated with superficial infections are not so limited as surface temperatures of the human body are lower than the core body temperature.
Geographic Region Highlighted
In selecting the tropical Asian and Oceania region as the focus of this study, I am concentrating on the general region of the world where information gathering has been less intense and the details are often hidden in more general texts. It also is representative of the region where most of my scientific career has been spent—tropical Australia, Papua New Guinea and Thailand.
The tropics comprise the zone bordering the equator stretching from the Tropic of Capricorn (southern hemisphere or latitude approximately 23.3 degrees south) to the Tropic of Cancer (northern hemisphere or latitude approximately 23.3 north). The Tropic of Capricorn passes through Australia (northern third commencing at Rockhampton in Queensland). In the northern hemisphere the Tropic of Cancer passes through India (southern half—line passes close to Ahmadabad—and West Bengal), Bangladesh (coastal delta with the line passing south of Dhaka), Myanmar (southern two thirds), the three southern provinces of China (Yunnan, Guangxi and Guangdong), and the southern half of Taiwan (commences at Chianyi city). It has not always be possible to determine whether a report from a country relates precisely to the tropical or subtropical region due to the lack of detail provided; this means that some reports from India and Taiwan may be grouped somewhat incorrectly. In reality, then, the study area embraced is the tropics and associated areas. Of course all readers will recognize that microbes do not recognize latitudinal lines, although some do occupy geographic zones of preference (cf. Walker 1996).
Tropical Asia consists of segments of South and East Asia and Southeast Asia. South Asia has at its core India, Bangladesh, Myanmar and Sri Lanka in the tropical zone. The People's Republic of China (three southern mainland provinces and Hong Kong) and Taiwan are part of East Asia. They fit into the tropics as do the Southeast Asian countries—Laos, Cambodia, Peninsular Malaysia, Singapore, Thailand and Vietnam. The tropics include Brunei, Indonesia, Sabah, Sarawak, Philippines and the smaller Pacific Islands (those just south of Necker Island, Hawaii to the equator and south of it to and including New Caledonia, French Polynesia, and Tonga)—the oceanic region separated from continental Asia is sometimes referred to as Oceania. In this account the term tropical Oceania is taken to incorporate the tropical zone between Asia and the Americas.
The Villains: Some Significant Pathogens
At the outset, it must be stated that pathogenicity is rare among the fungi. Most live a secret life of usefulness. The fungi involved as human and animal pathogens may be classified as primary pathogens or as opportunistic. Among the latter is a group of rarely encountered organisms. The following Table highlights this information with the emphasis on human diseases, but it is not meant to be exhaustive for the countries in the zone under consideration. By convention the yeasts often are separated from the fungi. The latter are organisms with a predominant filamentous or hyphal habit, although readers will recognise that both fungi and yeasts are eukaryotic and are found in the kingdom Fungi. I have included one water mould in our discussions. This organism, a Pythium, previously enjoyed a place with the fungi, but now it is classified in a different kingdom (Stramenopila). It is included at the risk of losing information about this significant pathogen.
One of the confusing aspects of working with fungi is that some organisms carry two names. This has come about since many fungi reproduce by both asexual methods (anamorphic—no union of nuclei involved) and sexual means (teleomorphic—union of two nuclei involved). To illustrate, if the anamorphic form of a fungus is discovered first, it is named according to its perceived morphologically similar relatives and placed in a form-genus or artificial genus. Later if the teleomorphic form is discovered its relationships became clearer and it is named accordingly (some genera are known solely by their sexual structures). The International Code of Nomenclature dictates that the whole fungus should be named after that of the teleomorph where it is known (Kirk et al. 2008). However, all this will change in 2013 when a fungus will be known by one name. Generally the whole fungus (holomorph) will take the teleomorph name, but under some circumstances it can take the anamorph name (Hawksworth 2011). In this account, where both asexual and sexual reproduction is known and an organism has two names, we will give both anamorph and teleomorph names at the first mention of the fungus in a chapter and then will refer to it by its holomorph name when this is reasonably well established. The time schedule for name changes is in the immediate future, but it will take some time for names to become settled.
About one fifth of fungal species classified among the two great phyla Ascomycota and Basidiomycota (sub-kingdom Dikarya) are known by their asexual structures, but this is not to infer that they lack sexual reproduction even though it may not yet have been found (Shenoy et al. 2007, Hyde et al. 2011, Taylor 2011). With the advent of DNA technology, the relationships among fungi have been revolutionized and in the near future they will become clearer. As this happens, some species will be moved to other genera. These changes will make information gathering more complex at one level and easier at another.
Some organisms are known by their asexual fruiting bodies alone. These have been placed into an artificial group known as the Deuteromycetes or Anamorphic fungi. This is a classification of convenience. Within this grouping, various subgroupings are made to help scientists in their identification. These groupings do not suggest genetic relationships. Indeed, a morphological species may be separated into a number of phylogenetic species using DNA technology, which makes statements about the ecology and disease-eliciting potential of a number of fungi problematic (Shenoy et al. 2007).
Before we enter into a brief discussion of taxonomy, I have listed some fungi and fungal-like organisms that have been shown to be pathogenic somewhere in the geographical area of emphasis (Table 1.1). These have been organized mainly under descriptive headings and some under distinctive classification groupings. We will deal with classification issues more fully in the next section.
Many more fungi than listed under each grouping have been found to be pathogenic (Ellis et al. 2007, Ellis 2011). Other fungi are being added to the list continually; although it must be stated that Koch's postulates have not always been satisfied for such candidates. In Table 1.1 the ascomycete now known as Pneumocystis jirevecii (previously P. carinii) is highly significant among the immunocompromised. Closely related species are found in many mammalian species (Cushion et al. 2004). Other fungi mentioned as human pathogens also are pathogenic to plants (e.g., Colletotrichum dematium, Lasiodiplodia theobromae, Nattrassia mangiferae) and still others infect both mankind and a variety of animals. The vast majority are saprophytic in nature and are not dependent on an animal or plant host for completion of their life cycle. Some have intimate relationships with plants, animals and specific organic substrates. We will mention some of these associations in later chapters.
Restricting the area of interest to the tropics reduces the consideration of some disease states as these have not been recorded there. For example, north India is an endemic region for paranasal sinus infections among young farmers caused by a wide variety of fungi (Chakrabarti & Sharma 2000); we will not consider these infections in any detail as they occur most intensely outside the tropics. A wide range of fungi may also be involved in corneal ulceration over the geographic region of interest—such occurrences have multiple causes (e.g., Srinivasan et al. 1997; Gopinathan et al. 2002). It is mostly beyond the scope of this study to give consideration of all the fungi thought to be involved in ulceration. One example is mentioned in the Table 1.1—corneal ulceration caused by Colletotrichum dematium—in order to give another example of a fungus from the form-group known as the Coelomycetes (Mendiratta et al. 2005).
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Table of Contents
Chapter 1: Introduction....................1
Chapter 2: Old Treats....................17
Chapter 3: Fungal Toxins, Cell Components and Health....................42
Chapter 4: New Challenges....................55
Chapter 5: Patterns of Reproduction....................76
Chapter 6: Mechanisms Available for Adaptation....................94
Chapter 7: Microbial Ecology....................111
Chapter 8: Habitat Relationships....................143
Chapter 9: Virulence and Related Factors....................161
Chapter 10: Mycotoxin Risk Minimization....................188
Chapter 11: Fungal Control through Host Modification and the Use of Microbes....................209