Numerous pathogens can be found in the soil.
\r\n\t
\r\n\tSince they involve very small amounts of energy, high sound pressure levels are increasingly simpler and cheaper to emit. Noise is everywhere - it can be emitted as an energy waste by traffic or factories, but also by teenagers looking for loneliness in an overpopulated world.
\r\n\t
\r\n\tWhen the noise emission ends, it will not be possible to find its footprint in the environment, hence it is necessary to be in the right place at the right time to measure it. Moreover, having adequate instruments, updated protocols and trained personnel are mandatory to achieve that. Even then, decision makers must clearly understand the reported situation to decide the need and importance of taking further actions.
\r\n\t
\r\n\tThis book will address issues of noise in the city, in the neighborhood or at work, aspects about management and consequences of exposure to high sound pressure levels ranging from the auditory, extra-auditory and psychophysics effects to the addiction to noise and the loss of solidarity.
\r\n\t
\r\n\tThe book aims to provide a various points of view and analysis of cases regarding this omnipresent pollutant.
Contrasts between two entities may be illuminating because of the emphasis on what each is not. Here we describe two proteinopathies producing brain neurodegeneration in mature adults, autosomal dominant valosin-containing protein (VCP) disease and Familial Alzheimer’s disease (FAD) caused by presenillin-1 (PSEN1) mutations, illustrating both contrasting patterns of clinical presentation and known neuropathologic and imaging features, and points of congruence.
Mutations primarily in the ubiquitin binding domain of the VCP gene cause frontotemporal dementia as part of a rare but important disorder that also encompasses inclusion body myopathy, Paget disease of bone, and in some cases, motor neuron disease. The VCP dementia has onset in the 50s, characterized by abulia, expressive language loss, and executive dysfunction. The pattern of degeneration generally is anterior, in frontal and temporal lobes, involving neuronal nuclear inclusions of ubiquitin and TAR DNA binding protein 43 (TDP-43), but not amyloid or tau.
The most common mutations causing FAD occur in the PSEN1 gene. The associated dementia has onset in the late 40s, characterized by early memory loss and diffuse amyloid vasculopathy, and posteriorly distributed neuritic amyloid plaque and neurofibrillary tau pathology in medial temporal and parietal lobes, but not ubiquitin or TDP-43. Nonetheless, both VCP and PSEN1 pathologies have extensively documented abnormalities in similar protein processing pathways.
Hereditary inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia (IBMPFD; OMIM 167320) is a unique and rare disorder associated with mutations primarily in the ubiquitin binding domain of the valosin-containing protein (VCP) gene (Watts et al. 2003; Watts et al. 2004). VCP, a member of the AAA-ATPase super-family, occupies the crossroads of many cellular functions including ubiquitin mediated protein degradation, cell cycle control, membrane fusion, and golgi reassembly (Kimonis and Watts 2005; Halawani and Latterich 2006). It is lethal as a homozygous deletion in mice (Muller et al. 2007), and an important regulator of neuronal and dendritic development (Rumpf et al. 2011).
Current theories concerning the pathogenesis of VCP disease include altered protein degradation via the ubiquitin-protosomal system (Kakizuka 2008; Dai and Li 2001; Wojcik, Yano, and DeMartino 2004), generalized endoplasmic reticulum (ER) dysfunction with altered protein trafficking (Weihl et al. 2006; Wojcik et al. 2006; Poksay et al. 2011), and combined activation and failure of inhibition of cell death pathways (Braun and Zischka 2008). Recently VCP has been implicated in the autophagy/lysosome process (Badadani et al. 2010; Ju et al. 2009; Ju et al. 2008; Ju and Weihl 2010a, 2010b; Tresse et al. 2010). These studies have suggested that VCP mutations cause failure of autophagosome fusion with lysosomes, resulting in accumulation of ubiquitin together with other autophagosome proteins LC3 and p62/sequestosome, in rimmed vacuoles, a hallmark of VCP muscle disease (Vesa et al. 2009, Ju et al. 2009; Tresse et al. 2010).
Certain mutations are also suspected to interrupt the integrity of the hexomeric ring structure of the active VCP complex (Halawani et al. 2009), and its interaction with its adaptors, e.g. p47, gp78 and Npl4-Ufd1 (Alzayady et al. 2005), although this finding has not been universally replicated (Weihl et al. 2007). Our group has confirmed that mutant VCP protein exhibit strongly altered co-factor interactions suggesting that imbalanced co-factor binding to p97 is a key pathological feature of IBMPFD and potentially of other proteinopathies involving VCP (Fernandez-Saiz and Buchberger 2010). Elevated ATPase activity associated with cellular protein mislocalization (Manno et al. 2010) is associated with VCP mutations. Recently studies revealed significant reduction in ATP level in hs.TER94A229E and hs.TER94R188Q drosophila models which may contribute to the neurodegeneration phenotype (Chang et al. 2011, Ritson et al. 2010).
The R155H VCP knock-in heterozygous mouse is a promising model demonstrating several typical clinical and molecular features of the disease including progressive weakness, vacuolization of myofibrils with centrally located nuclei, and cytoplasmic accumulation of TDP-43 and ubiquitin in brain as well as in myofibers (Badadani et al. 2010; Custer et al. 2010). It may prove to be very useful in translational research studies seeking therapies for VCP disease. Analysis of a Drosophila model has provided evidence that mutant VCP interacts abnormally with TDP-43 as a gain-of-function mechanism to cause redistribution of TDP-43 from its usual location in the nucleus to the cytoplasm (Ritson et al. 2010). These findings would be usefully replicated in the mouse model.
The clinical disorder typically presents in the early 40s with progressive proximal muscle weakness or with Paget disease of bone (PDB). Weakness is associated with rimmed vacuoles and inclusions on muscle biopsy in the majority of individuals; PDB is present in approximately half of affected individuals. Frontotemporal dementia (Table 1) becomes symptomatic later in a third of affected at a mean age of 55 years (Kimonis and Watts 2007; Kimonis, Fulchiero et al. 2008; Kimonis, Mehta et al. 2008; Kimonis and Watts 2005; Kovach et al. 2001). A small percentage of individuals have been identified with motor neuron disease (MND) phenotype (Johnson et al. 2010), Parkinson’s disease (Johnson et al. 2010; Rohrer et al. 2011), cardiomyopathy (Hubbers et al. 2007; Miller et al. 2009), liver disease (Guyant-Marechal et al. 2006), cataracts (Guyant-Marechal et al. 2006), hearing loss (Djamshidian et al. 2009), or corticospinal tract dysfunction (Kumar et al. 2010).
The VCP disease-associated dementia typically presents with frontotemporal phenotypes, e.g., altered social behavior, abulia, executive dysfunction, altered expressive language, and loss of semantic knowledge (Table 1). However, different families carrying the same VCP mutation may have a wide variation in clinical phenotype. For example, some families carrying the R159H VCP mutation may have an apparent high penetrance for the dementia phenotype (frequency 75-100%; van der Zee et al. 2009) but different average ages of onset (46 ±2 vs. 62 ±1 years). Other families with R159H may express high penetrance of PDB and IBM phenotype (100%) but demonstrate relatively low dementia frequency (20%; Haubenberger et al. 2005). The presenting dementia phenotype in R155C VCP may be behavioral variant FTD, an AD-like memory loss, or a non-specific cognitive dysfunction across several domains (Guyant-Marechal et al. 2006).
Some of this variability may have to do with the interest and specialty expertise of the clinics in which affected patients are seen, e.g., increasing the likely detection of FTD in a clinic dedicated to this sometimes difficult to diagnose disorder. The age at which the patient is seen and the length of follow-up will determine the presence and degree of cognitive and behavioral symptoms, and thus the likelihood of meeting criteria for a clinical diagnosis. Early memory symptoms may evolve into a more recognizable behavioral syndrome typical of FTD (Guyant-Marechal et al. 2006; Krause et al. 2007; van der Zee et al. 2009). Relative timing of the symptoms of FTD, PDB and IBM may also influence observed phenotypic frequencies – severe muscle disease with cardiomyopathy and respiratory failure might occur before dementia could be observed. Early dementia symptoms could be misinterpreted as a medical complication of severe respiratory or cardiac illness.
Nonetheless a substantial biologic variability across and within families with the same mutation, and across mutations, is well documented in VCP dementia. Potential explanations for variability are modifier genes, epigenetic mechanisms, and environmental exposures, the latter two possibilities as yet unexplored. A possible modifier gene is apolipoprotein-E. Possession of one or more APOE4 alleles was found to be associated with dementia in VCP disease, and increases risk for sporadic FTD in a dose-dependent manner (Bernardi et al. 2006; Mehta et al. 2007; Rosso et al. 2002). Tau haplotype was not associated with VCP dementia (Mehta et al. 2007), and VCP polymorphisms have not been found to be increased in the general population of patients with sporadic FTD (Schumacher et al. 2009).
Despite variability in clinical presentation, the qualitative pathologic changes are relatively uniform (Table 2). Post-mortem brains of individuals with VCP mutations reveal 75% have findings pathologically classified as frontotemporal lobar dementia ubiquitin type (FTLD-U), with abundant intranuclear ubiquitinated protein inclusions, dystrophic neuritis and rare cytoplasmic ubiquitin-positive inclusions (Forman et al. 2006; Kimonis, Fulchiero et al. 2008). Possible exception to this relative uniformity is the finding of vacuolar change in frontotemporal regions but not intranuclear ubiquitin pathology in three autopsies of R155C VCP mutation patients (Guyant-Marechal et al. 2006). This apparent anomaly may have a technical basis, since two of these subjects had increased frontal lobe ubiquitin immunoreactivity on Western blot.
Intranuclear inclusions of ubiquitin co-localized with TDP-43 are widespread and numerous
Dementia in VCP disease. Columns (left to right): 1. Reporting 1st author, 2. Mutation, 3. Number with dementia/ total reported, 4. Average dementia onset age (number reported), 5. Clinical Dementia type (number of each reported), 6. Affected with muscle disease/ total affected, 7. Affected with Paget disease of Bone/ total affected, 8. Additional comments
Neuropathology in VCP Disease. Columns (left to right): 1. Reporting 1st author, 2. Number reported, 3. Mutation, 4 - 8. Intensity of regional pathology (subjective, relative, not quantitative); MT – medial temporal), 9-10. TDP-43 Pathology (Nu – intranuclear, Cyt – cytoplasmic), 11-12. VCP Pathology, 13. Ubiquitin staining, 14. Neurofilament staining, 15. Tau Pathology, 16. Alpha-synuclein staining (aSN), 17. Polyglutamine Pathology, 18. Beta-amyloid staining, 19. Additional comments (AHC – anterior horn cell).
in cortical and basal ganglia, sometimes with a “cats-eye” curvilinear morphology (Neumann et al. 2007; Neumann, Tolnay, and Mackenzie 2009). Dystrophic neurites and cytoplasmic inclusions are relatively low in number in VCP disease brain and contain both proteins. TDP-43 appears to be depleted in normal neuronal nuclei (Neumann et al. 2007). The distribution of protein pathology and neuronal loss may be diffuse and include the occipital lobe, but when focal is predominant in the frontal and temporal regions, sometimes asymmetrically to right or left. The medial temporal lobe, particularly the dentate gyrus, is mostly spared. Occasional coexistent tau, alpha-synuclein, or amyloid pathology is detectible in some cases but this is not characteristic. Some authors have reported VCP within inclusions (Schroder et al. 2005), but others have found it only rarely in dystrophic neurites (Forman et al. 2006). Other pathologies, e.g., neurofiliment or polyglutamine, are absent.
TDP-43 has also been identified as the major disease protein in the ubiquitin-positive inclusions of sporadic and familial FTLD-U, including patients with the MND phenotype (Cairns, Neumann et al. 2007). These pathologic features overlap with those of amyotrophic lateral sclerosis. Anterior horn cell loss has been observed on spinal cord examination in some affected subjects with VCP mutations (Liscic et al. 2008), and the MND phenotype has been described as a dominant feature in a family carrying the R191Q VCP mutation (Johnson et al. 2010). In VCP disease, the pathologic classification best fits the description of FTLD-U, type 4 (Sampathu et al. 2006), distinguished by the intracellular localization of the inclusions, relative rarity of cytoplasmic inclusions and dystrophic neurites, and sparing of the medial temporal lobe, particularly the dentate gyrus. The question of whether the neuropathologic features in VCP disease with MND phenotype most resemble FTLD-U type 4 or FTLD-U types 2 and 3 associated with sporadic FTD with MND phenotype, characterized by abundant cytoplasmic inclusions, remains to be answered. Although rare, VCP disease may provide new insight into the molecular mechanism of TDP-43 proteinopathies caused by more common genetic alterations.
Imaging studies of the brain in VCP mutation carriers with cognitive alterations have also demonstrated variability (Table 3). However, few studies have been performed. The variability in part is due to use of differing imaging modalities: structural computed tomography and magnetic resonance imaging, and functional resting fluorodeoxyglucose positron emission tomography (regional glucose uptake; FDG-PET) and single photon emission tomography (regional perfusion; SPECT). These studies have been performed in different combinations and at different stages of cognitive impairment.
Imaging performed in the presence of subtle cognitive changes thought to presage dementia demonstrates no structural change (Kalbe et al 2011; Djamshidian et al 2009; Watts et al. 2007) and occasional subtle regions of glucose hypometabolism (Kalbe et al. 2011). In subjects with dementia, when present local cortical atrophies may be symmetric in the frontotemporal regions (Watts et al. 2007, Miller et al. 2009, Krause et l. 2007, Schroeder et al. 2005, Rohrer et al. 2011, van der Zee et l. 2009) or lateralized to the right or left with an anterior temporal emphasis (Kim et a. 2011). Other structural studies may show only generalized atrophy (Gidaro et al. 2008, Watts et al. 2007, van der Zee et al. 2009, Guyant-Marechal et al. 2006). Hypoperfusion (SPECT) and glucose hypometabolism (FDG-PET) generally correspond to the regions of greatest atrophy seen on structural imaging in the same patients.
Imaging in VCP disease. Columns (left to right): 1. Reporting 1st author, 2. Mutation, 3. Modality used, 4. Presence of focal atrophy, (number/ total images reported), 5. Generalized/diffuse atrophy pattern (number/ total images reported), 6. Presence of white matter hyperintensities or other abnormalities (number/ total images reported), 8. Additional comments.
Autosomal dominant familial Alzheimer\'s disease (FAD; OMIM 104300) is usually of early onset (EOAD; age < 65 years) and has been known for many years (Janssen et al. 2003). Alzheimer\'s original case description was reported because of the observed early onset of disease at age 51; before then "senile dementia" was thought only to occur in the elderly (Maurer, Volk, and Gerbaldo 1997). Most cases of FAD are attributable to mutation of the PSEN1 gene on chromosome 14 (OMIM 104311; Campion et al. 1999). The remaining cases are found in rare families harboring mutations in amyloid precursor protein (APP) on chromosome 21, in presenillin-2 (PSEN2) on chromosome 1, or with a currently unknown genetic substrate, including overlap with a small part of the Bell curve continuous with late onset AD (LOAD; Brickell et al. 2006).
Here the focus is on PSEN1-related FAD because it is by far the most frequent FAD type and hence more is known about these families. Presenilin-1 is an important component of the gamma-secretase that cleaves amyloid precursor protein (APP) and NOTCH. It is involved in adult neuronal stem cell differentiation (Gadadhar, Marr, and Lazarov 2011), early cortical development (De Gasperi et al. 2008; Wines-Samuelson and Shen 2005), endoplasmic reticulum calcium regulation (Coen and Annaert 2010), and autophagy (Lee et al. 2010). There are currently 194 known PSEN1 mutations (
The spectrum of phenotypic and neuropathologic variation is even wider when different mutations are considered. For example a variant with dementia associated with spastic paraparesis is associated with several PSEN1 mutations: deletion in exon 9, insertion in exon 3, P436Q, R278K, G217R and L85P point mutations, and deletion of codons 83 and 84 in exon 4 (Verkkoniemi et al. 2000; Houlden et al. 2000; Moretti et al. 2004; Ataka et al. 2004; Assini et al. 2003; Smith et al. 2001; Norton et al. 2009). Neuropathology of these variants includes characteristic fluffy spheres of non-neuritic extraneuronal amyloid termed cotton-wool plaques (Houlden et al. 2000). In one patient with a small deletion in PSEN1 exon 12, parkinsonism, spasticity and dementia were the clinical features and neuropathologic examination showed cotton-wool plaques, cortical and subcortical Lewy bodies, and extensive amyloid angiopathy (Ishikawa et al. 2005). Prominent periventricular white matter hyperintensities associated with spastic paraparesis have been observed on MRI in two E280G and in four P284S PSEN1 mutation carriers (O\'Riordan et al. 2002; Marrosu et al. 2006). Extensive amyloid angiopathy causing white matter ischemia could explain the paraparesis in these cases.
Clinical studies of PSEN1 mutation kindreds have reported widely variable age of onset, e.g., 28 years in a de novo M233L mutation carrier (Portet et al. 2003) and a range of onset within the same H163T mutation family of 44-65 years (Axelman, Basun, and Lannfelt 1998). Clinical findings can also include, prominent psychiatric symptoms (S170F mutation (Piccini et al. 2007); L392P (Tedde et al. 2000)), a behavioral variant frontotemporal dementia syndrome (bvFTD; L113P(Raux et al. 2000)), anomia (R278I(Godbolt et al. 2004)), seizures and myoclonus (S170F(Snider et al. 2005), cerebellar ataxia, intention tremor, and dysdiadochokinesia. Neuropathologic findings are generally robust depositions in the form of A-beta1-42(3) and A-beta1-40 amyloid in vessels, sometimes extending into parenchyma and termed dyshoric vasculopathy, neuritic plaques, tau-laden neuropil threads, and hyperphosphorylated tau protein forming intraneuronal tangles within cortical neurons (Janssen et al. 2000; Janssen et al. 2001). Pathologic, brainstem and cortical Lewy bodies (Kaneko et al. 2007; Snider et al. 2005), and possibly Pick-type tauopathy has been found in carriers of the PSEN1 G183V and M146L mutations (Dermaut et al. 2004; Halliday et al. 2005). TDP-43 and ubiquitin are not seen.
A large kindred identified in Columbia, South America is the focus of an ongoing large scale study of AD in its earliest, pre-symptomatic stages, serving as a model for the much more frequent LOAD (>95% of all AD cases; Lopera et al. 1997; Acosta-Baena et al. 2011). The causative mutation is E280A. Onset age in the initial study was an average 47 years, but there was a wide range between 34 and 62 years. The average life span following diagnosis was 8 years (Lopera et al. 1997). Longitudinal follow-up has shown that the earliest detectible cognitive changes occur at average age 35 years, progressing through mild stages of impairment associated with memory complaints to dementia over approximately 15 years. Time from dementia to death is now estimated as 10 years, likely due to improved methods of early detection and diagnosis as the study has developed (Acosta-Baena et al. 2011). Studies in this kindred using hexamethylpropyleneamine oxime SPECT has demonstrated decreased perfusion in hippocampus, posterior cingulate, and frontoparietal cortex in asymptomatic carriers (n=18) using t-scores based on a template derived from 200 normal subjects. Carriers with diagnosed AD dementia (n=16) had decreased frontal and parietal perfusion compared to normal non-carriers from the same kindred (n=23). The clear major advantages for the study of this kindred is its large size (449 identified mutation carriers), a cognitive phenotype that parallels LOAD, and the very high predictability of dementia in PSEN1 carriers. In contrast, LOAD has no genetic profile or multivariate model that can approach the predictive power of an autosomal dominant mutation.
At the most general level cortical regions most affected by VCP-associated pathology are connected by the anterior 60% of the corpus callosum and the anterior commissure – the prefrontal, orbitofrontal, premotor and anterior temporal cortices. Anterior horn cells and muscle share the ubiquitin/TDP-43 pathology. Long tract findings are exceptional. The clinical syndromes associated with cortical dysfunction in these regions fall broadly into the class of frontotemporal dementias, and encompass behavioral, dysexecutive, expressive language, and semantic access symptom cores. In brain the characteristic ubiquitin/TDP-43 inclusions are neuronal intranuclear and rarely cytoplasmic or extracellular. The medial temporal lobe, particularly the dentate nucleus, is largely spared. Tau and amyloid pathology are not found. Imaging reveals commensurate frontotemporal atrophy, sometimes lateralized in correlation with the clinical syndrome, accompanied by hypometabolism and hypoperfusion in these anterior regions.
In contrast, cortical regions most affected by FAD PSEN1-associated pathology are connected across the posterior 40% of the corpus callosum and posterior hippocampal commissure – the parietal, superior and inferior temporal lobes and medial temporal lobes but generally sparing the primary occipital region. Neuropathology is described as quite dense and parallels that found in LOAD, e.g., include extracellular neuritic plaques, cytoplasmic fibrillary tangles, neuropil threads and amyloid angiopathy. The temporal lobe, particularly the medial portion is heavily affected. Ubiquitin and TDP-43 are absent. In many cases a classic AD clinical sequence of early memory loss followed by declines in other cognitive domains is described, particularly well documented in PSEN1 E280A families. Variants include EOAD with spastic paraparesis, characteristic “cotton wool” extracellular amyloid plaques and dense amyloid angiopathy. Involvement of the lower motor neuron has not been reported. Structural imaging reveals atrophic changes in temporal and parietal lobes, with hypometabolism, particularly in posterior cingulate and other parietal areas.
Both VCP disease and FAD PSEN1 are single-gene disorders producing dementia phenotypes similar to those seen much more frequently in sporadic disease. In both there is marked variation in phenotypic expression of the same mutation within and across families, and across mutations in the same gene, with overlapping presentations of the FTD or AD dementia phenotypes between genes in some cases. Both VCP and PSEN1 genes have dual roles in both CNS development and in maintenance of the mature nervous system, but produce neurologic dysfunction only in the adult associated with characteristic protein accumulations. Finally both VCP and PSEN1 pathophysiologic alterations appear to overlap at several points within cellular protein processing and functional pathways, including protein trafficking in the trans-golgi apparatus, downstream in the ubiquitin-proteosome system, and autophagy (Table 4. )
Neuropathologic Features and Points of Comparison: IBMPFD vs. FAD.
VCP disease and FAD PSEN1 appear to have commonalities at a fundamental level in that both involve altered polyfunctional proteins involved in specific overlapping functions, particularly autophagy, and have common downstream pathways, e.g., proteosomal. Yet the diseases are clearly distinct in most particulars, suggesting a principle of independent compartmentalization that may provide insights into both disorders.
The definition of soil according to the sciences of the earth and life points to the external part of the earth’s crust, which is biologically active and tends to develop on the surface of the rocks emerged by the influence of weather and living beings. It is also frequent that this concept includes a complex set of physical, chemical, and biological elements that make up the natural substrate in which life develops on the surface of the continents. The soil is the habitat of a specific biota of microorganisms (bacteria and fungi), plants, and small animals that constitute the edaphon.
In recent decades, there has been an increasing concern for soil biodiversity, on the basis that the interactions between microorganisms, animals, and plants provide an undoubted benefit to the well-being of mammalian species, including man [1]. This biodiversity conditions both the possibilities of feeding these species, oxygenation, as well as the control of the risk of certain diseases. For these reasons, it is not difficult to understand that soil biodiversity is directly affected by global changes caused by man, especially those related to land use, urbanization, agriculture, deforestation, and desertification, which leads to the logical conclusion that the careful and sustainable use of soils would guarantee their benefits.
Different studies have indicated that exposure to soil microorganisms decreases the prevalence of allergic diseases [2]; taking into account the predictions that around the year 2050 two-thirds of the world population will reside in cities, the stimulation of the immune system by soil organisms will be reduced, and therefore allergy cases will increase.
Other researches highlight the increase in the appearance of bacterial species resistant to most known antibiotics, and the same happens with some parasites, such as helminths. The use of remedies found in the soil, such as certain types of fungi, has not yet come to be considered as a solution to the aforementioned problems. It is interesting to know that some bacteria capable of synthesizing effective antibiotics against Mycobacterium tuberculosis have been isolated in the soil [3]. It should also be noted the production of molecules with parasiticide action from fungi [4]. Special mention should be made of the use of some fungal species in the control of certain endoparasites that, once in the soil, complete a series of phases until they reach the infective stage [5]. In recent years, very important achievements have been made in the large-scale production of saprophytic fungal spores that are found in the soil, such as Mucor circinelloides or Duddingtonia flagrans, filamentous species that are in contact with eggs or larvae of some parasites, respectively. They have the capacity to destroy them or limit their viability [6, 7]. In this way, it is possible to reduce the risk of infection in people, and also in animals that are in pasture.
Pathogenic organisms belong mainly to five main groups, viruses, bacteria, fungi, and parasites (protozoa, helminths, and ectoparasites) [8]. From an academic and disease control approach, the importance of soil lies in the fact that a significant number of pathogens are found in this habitat, and sometimes they are accidentally ingested by animals and people, causing important disorders. There are some organisms that do not require ingestion, being able to spread their pathogenicity through bites or penetrating the skin.
Table 1 summarizes different examples of pathogens present in the soil. It is important to note that most soil organisms do not constitute a health risk, and pathogenic species represent only a minority. Nor should we forget that some species are opportunistic (Pseudomonas and Enterobacter) and can cause alterations in mammals, although in the soil they are actually antagonists of root pathogens of some plant species, or can act as growth promoters of some plants and even as decomposers of organic matter [9]. Other pathogens need to develop part of their cycle in the soil, to complete their evolution until the infective phase. These are organisms that can survive in the soil for long periods of time, and include spores, eggs, or even larvae. These are obligate pathogens that temporarily reside in the soil, and that are transmitted to mammals by direct contact, by vectors, or through accidental ingestion [10]. For these reasons, it is necessary to know the ecology of the interactions between the soil and the various organisms to determine why some are prevalent and persist under certain conditions.
Bacteria | Bacillus anthracis | Agrobacterium tumefaciens |
Listeria monocytogenes | Escherichia coli | |
Salmonella spp. | Clostridium spp. | |
Fungi | Aspergillus spp. | Histoplasma capsulatum |
Coccidioides immitis | ||
Protozoa | Naegleria fowleri | Toxoplasma gondii |
Helminths | Ascaris spp. | Taenia spp. |
Ancylostoma spp. | Strongylus spp. | |
Ectoparasites | Pulex irritans | Ixodes spp. |
Numerous pathogens can be found in the soil.
The concept of Soil Borne Human Diseases offers a very accurate introduction about the role that soil can play in the transmission of certain diseases [11]. However, it is obvious that this idea is a bit limited, since not only the human species will experience the risk of contracting diseases from this habitat. From an etiological point of view, pathogenic organisms are defined as those whose habitat is the soil, and pathogens transmitted by the soil as organisms that can survive for long periods of time in the soil, and need to do so to infect the host and continue their biological cycle, but they are not part of the soil [12]. Some of the most frequent endoparasites affecting people and animals, such as roundworms, cestodes, or strongyles, belong to this group, and they are characterized by undergoing a series of changes in the soil to the infecting stage. Part of the biological cycle of some ectoparasites such as fleas or ticks occurs in the soil also. This underlines the importance of soil as an adequate medium to certain parasites can survive and develop to infective stages, pending of proper hosts ingest them (flatworms, roundworms, whipworms), contact with soil (hookworms) or walk near (ectoparasites). Regardless of their origin (animal/human), control of parasites affecting mammals requires some action on the stages in the group, since parasiticide therapy acts on the parasites living and affecting them only; thus, the risk of reinfection is elevated, even though successful treatments are applied.
Soil provides a suitable habitat to different organisms as plants can grow and develop, serving as food for the survival of many living creatures (insects and micromammals). This environment enables mammals as herbivores to graze and carnivores to find their feeding.
Most known parasites associated to soil are defined as soil-transmitted helminths (STHs), which involve well-known species belonging to flatworms, tapeworms, or roundworms. Helminths can develop a direct cycle in the soil, but an intermediate host is required for some species, and paratenic hosts participate in the transmission of several infections. On the basis of the zoonotic role of different parasites developing in the soil, it is necessary to know the external phase of their life cycle.
Transmission of STHs involves that eggs are passed in the feces of infected individuals. Once in the soil, flatworms (trematodes and cestodes) need to complete several stages inside an intermediate host, to attain the infective stage. Fasciola hepatica and Schistosoma mansoni (flatworms) are related to humid environments where a number of aquatic or amphibious snails take part. After some stages are completed and exit-off the snails, the infective stages known as metacercariae mature in herbage or water, and infection occurs by the ingestion of herbage or water contaminated [13].
Roundworms (Ascarids) represent the most spread nematodes around the world. Although these are host species-specific pathogens, humans can be involved as paratenic hosts for many of them such as roundworms infecting domestic animals (Toxocara canis, Ascaris suum) or wild species (Baylisascaris procyonis and Toxascaris leonina). Infection occurs by the accidental ingestion of larvated eggs (containing a second-stage larva inside) (Figure 1).
Numerous parasitic stages can be found in the soil (COPAR archive).
Whipworms (Trichuris spp.) have a similar cycle to roundworms. Transmission occurs by the oral ingestion of eggs holding a first larva.
In the case of Ancylostoma, nematodes (hookworms), embryonated eggs are passed in the feces and once in the soil, the first-stage larva (L3) emerges and molts to a second-stage larva and then to a third-stage larva, the infective stage. Infection can occur either by oral ingestion of L3 or through the skin [14].
It is well recognized that ticks need to suck blood from mammals for surviving, but sometimes it is forgotten that these ectoparasites develop part of their life cycle in the soil also. Gravid adult females drop off the final host to the ground to lay eggs. Under appropriate conditions, the egg hatches into a larva, which waits for an appropriate mammal to bite for feeding and then transform into nymph.
Appropriate conditions (moisture and temperature) must concur in the soil to improve the development of parasites to their infective stages. Nevertheless, evolution of parasites can be delayed until unfavorable circumstances appear, especially low temperatures. Some of them such as roundworms and whipworms are able to survive viable for long periods, even under temperatures below zero [15]. This resistance is conferred by their eggshells, composed of at least four layers, uterine (mucopolysaccharides), vitelin, chithinous, and lipidic (inner). Eggs of ticks can also survive in the environment unless the solar light falls directly on them.
Larval stages (first, second, or third) from nematodes exhibit a certain degree of resistance, and it has been reported they can subsist under snowy areas [16]. Dry soils in spite of very humid areas are preferred by immature hookworms [5], like sandy places. This explains the cutaneous infection of people enjoying outdoor activities on beaches, parks, etc. from touristic areas.
Human STHs are frequent in Asia, Africa, and South America, being absent in Western Europe and developed countries. Nevertheless, these diseases have reemerged due to immigration, travel, and business. Also in recent years, populations of ticks are increasing in urban areas, as well as orchards, parks, and gardens [17].
There are four main STHs affecting humans, Toxocara canis (roundworm), Ancylostoma duodenale and Necator americanus (hookworm), and Trichuris trichiura (whipworm). Between 1.5 and 2 billion people, it is believed that they are probably infected worldwide [18]. The presence of these parasites is associated to low standards of hygiene, poverty, and malnutrition because infection takes place by the accidental ingestion of eggs or through cutaneous contact with larvae of hookworms. It is necessary the exposure to feces of pets, mainly dogs. As advised by the WHO (World Health Organization), periodic administration of albendazole and mebendazole is helpful to reduce the incidence of these parasitoses. Deworming is the most applied measure against STHs, and extension of treatment (increment of frequency) looks like a valuable solution, although there is a potential emergence of drug resistance as observed in veterinary medicine [19]. By considering that infections originate from fecal contamination of the environment, mammals can become reinfected frequently after parasiticide treatment is administered. Consequently, actions on the environment are required to reduce the exposure to infective stages, mainly consisting of the use of latrines, together with hygienic behaviors.
Dogs are the definite hosts for T. canis and N. americanus, thus another question to address concerns the possibility of humans and animals sharing infections by parasites, the so-called parasitic zoonoses. As explained previously, transmission occurs in the same way, but the presence of infected animals becomes essential for human infection. In this case, control appears more difficult, due to the impossibility to ensure that pets receive an appropriate deworming therapy. The problem aggravates when considering that wild/uncontrolled animals can live near persons, because there is no way to perform control of their parasites by the administration of antiparasitic drugs. In some countries, it is not rare to observe feces of stray dogs or cats, foxes or raccoons, in private gardens, public parks, or even beaches. As stated above, humans might become infected by roundworms or hookworms, and despite infection, it is not completed, serious damage could be provoked attributable to the erratic migration of immature stages across the organism [20]. At this point, it seems necessary to remember that second-stage larvae of Toxocara canis (dog), T. cati (cat), Ascaris suum (pig), or Baylisascaris procyonis (raccoon) can cause a visceral larva migrans syndrome after these larvae are released at the gut level. Infection by T. canis can be responsible for an ocular larva migrans [21], while B. procyonis is associated to a devastating neurological syndrome, with children being the riskiest group due to their tendency to play with ground, or take and leave sand in the mouth [22]. The possibility of human infection through the exposure to eggs of roundworms on the coat of dogs has also been considered [23], which remarks the importance of these parasites are easily transmitted to their owners.
By considering that a great number of pathogens develop in the soil, one interesting question refers to why mammals did not infect more frequently, or why low to moderate infections are usually detected. Infection depends on the density of pathogens and risky situations such as accidental ingestion or active passage through the skin (helminths) or walking by places with vegetation (ectoparasites). Then, it could be expected that exposure to natural environments might represent a great hazard, thus enjoying natural habitats should be avoided (or even forbidden).
As mentioned previously, a great number of fungal species can be found in the soil, together with many other organisms such as viruses, bacteria, earthworms, insects, etc. Some of these species are saprophytic and feed on organic matter, but in the presence of parasitic stages such as eggs or larvae, they shift to predatory agents. Hyphae develop and the mycelium grows toward the parasites in an attempt to take certain nutrients, nitrogen and carbon mainly [24]. Other fungal species feed on different species of fungi, as succeeds with some mites.
It has been demonstrated that certain soil saprophytic fungi such as Duddingtonia flagrans are able to adapt to the numbers of larvae of nematodes developing from eggs shed in feces of infected grazing horses [25]. In the absence of nutrients, fungi can remain as resting stages (spores). It should be emphasized that different organisms interact simultaneously on the ground, thus soil fungi do not persist for long periods (4 months) and need to be replaced by new structures such as spores, mycelium, etc. [26]. This must be taken into account when soil fungi are going to be used under biological control strategies. Other interesting finding consists of the absence of activity on nonparasitic organisms (Figure 2).
Filamentous fungi develop hyphal nets in the soil, and reproduce by spores (COPAR archive).
Based on experiments with plants, traditionally the fungal antagonists of parasites comprise nematode-trapping species (larvicidal), predacious agents, endoparasitic fungi, and egg parasitic fungi (ovicidal) [27]. In the last decades, this classification applies also for defining the activity of soil fungi against parasites affecting mammals (Table 2).
Effect | Species | Action against | |
---|---|---|---|
Ovicidal | Pochonia chlamydosporia | Mucor circinelloides | Flatworms Roundworms (ascarids) Whipworms |
Purpureocillium lilacinus | Verticillium chlamydosporium | ||
Trichoderma spp. | Gliocladium spp. | ||
Larvicidal | Duddingtonia flagrans | Monacrosporium spp. | Hookworms Roundworms (strongyles) |
Arthrobotrys spp. |
Filamentous soil fungi antagonists of parasites in the soil.
In natural conditions, when the environment does not result altered by humans, soil albeits not only fungi but other microorganisms as viruses, bacteria, earthworms, insects… A number of filamentous fungi feed on organic detritus, certain coprophagous beetles participate in enriching the ground by decomposing organic matter as manure, some mites feed on fungi, and several fungi do it also. This means that an equilibrium situation takes place, where organisms are controlled mutually, and explains also why low risk of infection is usually observed. When agricultural procedures affecting the surface of the ground are performed, this habitat is transformed, and beneficial organisms drop or disappear. As a consequence, the density of pathogens increases, accordingly the risk of exposure among mammals increases and they can become infected.
Several investigations pointed the efficacy provided by some fungi to limit the viability of eggs of roundworms [28]. As drawn in Figures 3 and 4, the addition of spores of M. circinelloides to the feces of dogs infected by T. canis decreased their viability by half after a period of 30 days [29]. When the spores were sprayed onto feces of raccoons parasitized by B. procyonis, egg viability reduced by two-thirds also, in agreement with previous experiments [30].
Viability of eggs of Toxocara canis (left) and Baylisascaris procyonis (right) after 30 days of exposure to spores of Mucor circinelloides (Mucor30) or distilled water (Control 30). Points mean average values and bars the SD [29].
The soil filamentous fungus M. circinelloides is able to attach to the eggshells of roundworms such as T. canis, colonize, penetrate, and absorb the inner content (COPAR archive).
A notable efficacy has been reported against larvae of hookworms by using trapping-nematode fungi such as D. flagrans. A 57–73.2% reduction of the numbers of the third-stage larvae of Ancylostoma spp. has been obtained, and the counts of larvae decreased by 24.5–63% when exposed to chlamydospores of D. flagrans [31, 32].
By taking into account that the aforementioned parasites are STHs, the use of ovicidal and larvicidal fungi could be strongly helpful to limit the development of parasites to infective stages in the soil. One interesting question refers to the proper way to spread the fungi to ensure their contact with the parasites. Because the eggs of parasites are shed by feces, the most useful procedure looks to try that fungi are in the feces at the same time, and for this purpose, oral administration could be appropriate. Several investigations demonstrated that the spores of Pochonia chlamydosporia, Mucor circinelloides, and Duddingtonia flagrans can survive the passage through the gastrointestinal tract of different animal species, and retained their antagonistic activity [6, 33, 34]. Later, several assays were performed by adding spores or mycelium of Pochonia chlamydosporia or Duddingtonia flagrans during the handmade elaboration of nutritional pellets [35, 36, 37]. More recently, the capability of fungal spores to resist the industrial fabrication of pelleted feed has been demonstrated [38, 39]. The usefulness of pellets containing spores of M. circinelloides and D. flagrans has been tested on grazing horses, and highly successful results were obtained. Through this strategy, it was possible to reduce the frequency of deworming from 4 years to 1–1.5 years [7, 40]. This approach has also been assayed on wild captive equids maintained in a zoological park, and as a result the administration of anthelmintics was significantly lessened [41], supporting the results previously collected by administering the spores as a premixed feed [6].
It has been explained that ectoparasites develop part of their cycle in the soil. After mating on the host, gravid female ticks engorge completely and drop to the ground, where thousands of eggs are laid mainly in places protected from sun and desiccation, with vegetation. Later than a variable period, depending on temperature and humidity, eggs hatch and larvae exit off, addressing to plants, pending of a host to attach and suck blood for molting into nymphae. Beauveria bassiana and especially Metarhizium anisopliae are the most investigated entomopathogenic fungi capable of infecting and damaging ticks [42, 43]. Trials consisted of the topical administration of oil solutions, targeted against immature or adult stages [44]. The aim is to reduce the indiscriminate use of chemical acaricides, for avoiding contamination of food and environment, as well as the appearance of chemical resistance among tick populations [45].
There is little information available concerning the possible effect of fungi on tick eggs in the soil. Figure 5 summarizes the results collected after the exposure of eggs of Rhipicephalus boophilus to spores of M. circinelloides. The fungal activity was estimated by measuring the percentage of egg viability, and the hatching percentage, i.e., the percentage of larvae hatched after 15 days. Fungal growth started on the eggshells 4 days after exposure, and by 6 days, hyphae penetrated inside.
Viability of eggs of the tick R. boophilus exposed to spores of M. circinelloides (Mucor) or distilled water (Control). Points mean average values and bars the SD (COPAR archive).
Viability of ticks’ eggs decreased to 80% in the controls-untreated eggs, and to 38% in those exposed to the filamentous fungus. The hatching percentage was 45% in the controls, by 15% in the Mucor-treated eggs.
Four phases have been described during the activity that the ovicidal fungus Verticillium chlamydosporium perform on eggs of helminths, i.e., contact, attachment, penetration, and deliberation [46]. The fungus M. circinelloides develops a similar activity on both the eggs of helminths and ticks (Figure 6). When the spores contact with the parasites, hyphae grow toward the eggshell and colonize it. Those hyphae facing the eggshell in perpendicular are able to penetrate inside. This is possible due to the involvement of the appressorium, a pressing organ consisting of a flattened and thickened hypha, which is provided of a haustorium, a specialized branch which penetrates the tissues of the host and absorbs nutrients and water [47]. This mechanism enables the fungus to take all the inner content of the egg, without losing anything. Once completed, hyphae exit off and colonize other egg (deliberation).
Hyphae of M. circinelloides grow and attach to the eggshells of ticks, penetrate and destroy them (COPAR archive).
In view of the mentioned results, certain soil fungi seem very promising agents for limiting the viability and evolution of tick eggs in the soil, contributing to decrease the risk of infestation. One possible approach could rely on preparing aqueous solutions containing the fungal spores, and spreading by using airless sprayers. This would provide a solution to limit the risk of infestation in outdoor areas as waysides or the edge of grass along the roadsides, gardens, or even farms. Reduction in the presence of ticks in the soil also provides a sustainable and preventive tool to avoid damage to humans and animals.
Some strains of several soil fungal species have been isolated according to their ability to convert fungal oils into esters, providing thus a sustainable way to obtain biofuel [48, 49]. The interest of microbial oils has increased as they are now used as commercial sources of several nutritionally important polyunsaturated fatty acids [50].
Despite fungi being mostly considered responsible for fungal diseases that can range from nonsevere to mortal illnesses, fungal infections have become a serious health problem in immunocompromised patients largely.
Opposite to Duddingtonia flagrans and Monacrosporium thaumasium, the infection by Mucor circinelloides has been associated to clinical cases of mucormycosis, a sporadic and life-threatening infection caused by Mucorales. These are fungi distributed far and wide in the environment, in particular on woody surfaces and soils, where it can be easily isolated [27].
Several reports indicated nosocomial infection by M. circinelloides among immunocompromised people with skin wounds, or suffering diabetes mellitus [51].
Among animals, infection by M. circinelloides has been diagnosed in one Vietnamese potbellied pig presenting clinical signs of pneumonia, but information regarding the habitat or the level of inbreeding has not been provided [52].
Until now, long-term assays comprising the frequent administration (daily or twice a week) of a blend of spores of M. circinelloides and D. flagrans have been developed in pasturing horses. One group of seven horses received daily pellets containing the fungal spores during 64 weeks, and no adverse effects regarding respiratory, digestive, reproductive, or cutaneous damage were recorded [7]. Other group of eight horses was given pellets twice a week with the spores for a 1-year period, and after testing the activity of the respiratory, digestive, and reproductive systems, no alterations were recorded [41]. No signs of damage on skin integrity were observed.
Until now, there have not been reported any problem with people producing and managing spores/mycelium for longer than 10 years.
Inasmuch as STHs are transmitted through soil, it seems essential to develop measures on the environment to avoid reinfection, and the abusive administration of parasiticides. Some STHs originate from animals (domestic and wild), and helpful actions to reduce the risk of transmission are also required. Besides public education and hygienic behaviors, other activities should be applied to limit the presence and survival of infective stages of parasites. There have been described several species of soil fungi antagonists of eggs or larvae of helminths and ticks. Although several cases of disease have been linked to soil fungi, the absence of disease among people managing them or among animals receiving fungal structures seems to reinforce their safety, unless the patients are immunocompromised. The use of soil fungi against infections transmitted across ground gives a sustainable measure to prevent damage to persons and animals, and might allow us to limit the administration of antiparasitic drugs to imperative situations only.
This work was partly supported by the Research Project CTM2015-65954-R (Ministerio de Economía y Competitividad, Spain; FEDER). Dr. María Sol Arias Vázquez is recipient of a Ramón y Cajal contract (Spanish Ministry of Economy and Competitiveness), and Dr. C.F. Cazapal-Monteiro is beneficiary of a postdoctoral research fellowship (Xunta de Galicia, Spain).
All authors declare the absence of any financial or personal interests that could inappropriately influence or bias the current work. The final chapter has been approved by all the authors.
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