Chronic Environmental exposure to Alternaria tenuis may manifest symptoms of neuropsychological illnesses: A study of 12 Cases.

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Journal of Applied Sciences & Environmental Management, Vol. 9, No. 3,

2005, pp. 45-51

http://www.bioline.org.br/request?ja05057

Chronic Environmental exposure to Alternaria tenuis may manifest

symptoms of neuropsychological illnesses: A study of 12 Cases.

1*ANYANWU, E C; 2KANU, I, 1NWACHUKWU, N C; 1SALEH, M A

1Department of Chemistry, Environmental Toxicology Program, Texas

Southern University, Houston, Texas, USA.

2Department of Microbiology, AbiaStateUniversity, Uturu, Abia StateNigeria

Code Number: ja05057

ABSTRACT:

Toxigenic mold exposures are shown to lead to illnesses most of which

are just being unraveled. This paper reports the findings in cases of

12 white female office workers who presented with symptoms of

neuropsychological illnesses, most likely, due to indoor environmental

toxigenic mold exposures. Their major complaints were: weakness and

numbness in legs, dizziness, loss of memory, light-headedness and

vertigo, fatigue, getting lost in familiar territory, and confused

thoughts. The subjects were evaluated by testing immunologic, basic

EEG, and comprehensive neuropsychological tests. Abnormal antibodies

to Alternaria tenuis, Pullularia pullulans, and Epicoccum nigrum

antigens were found in all the subjects' serum, and they were quite

different from the abnormal levels of Aspergillus, Stachybotrys, and

Penicillium, Cladiosporium genera found in their indoor environment.

EEG examination was abnormal all the subjects with 10 Hz posterior

dominant activities in 6 out of 12, which were synchronous,

symmetrical and attenuated on eye opening and eye-closure. There was

an evidence of tremor of the extremities in 3 subjects. These

particular subjects' reflex was abnormal, and they had accommodation

paresis. Gross neuropsychological abnormalities including those

observed in the brain-damaged population and significantly below

non-brain damaged functioning was observed. These findings seem to

indicate that chronic exposures to Alternaria tenuis, Pullularia

pullulans, and Epicoccum nigrum might have neuropsychological effects,

and that most likely, only one abnormal antibody to toxigenic mold

antigen could have the most dominant adverse toxic exertion leading to

the observed neuropsychological effects. It is concluded therefore,

that chronic exposures to certain toxigenic molds might lead to

neuropsychological manifestations and that although, it is

acknowledged that the contaminations of the indoor environment by

toxigenic molds are directly related to the adverse health effects on

the occupants, there could be a situation where such relationship does

not exist. @JASEM

Indoor environmental air quality has taken a center stage in public

health discussions to which chronic exposures to toxigenic molds share

greater concerns than other indoor environmental contaminants. Hence,

there is increasing evidence of health risks associated with damp

buildings and homes in which high levels of toxigenic molds are found

to grow. Pieces of evidence are also accumulating that support the

views that certain toxigenic molds are particularly a risk factor for

adverse human health through exposure and inhalation of fungal spores

(Jarvis, 2002). Several residential homes are contaminated by these

toxigenic molds consequent upon which illnesses such as pulmonary

hemosiderosis in infants have been reported (Jarvis et al., 1996;

Flappan et al., 1999). It is also believed that such illnesses are

due, at least in greater part, to the mycotoxins produced by the

toxigenic molds. Although, the extent to which mycotoxins affect the

human health is still emerging, certain mold mycotoxins could be

contributory to a significant number of neuropsychological illnesses

than one would have imagined.

For infants, the elderly, and persons living or working in " at high

risk " urban areas the occurrence of illnesses due to toxigenic mold

exposures may be high, depending on the type of mold and the

individual health variations. However, what makes a full

understanding of the processes that lead to the action mechanism of

mycotoxins in humans very difficult is the fact that there are several

species of toxigenic molds that produce different toxic metabolites

that are capable of exerting different toxicological effects.

Cases of 12 white female office workers aged between 24 and 52 years

who presented with symptoms of neuropsychological illnesses, most

likely, due to indoor environmental toxigenic mold exposures were

comprehensively investigated. They all complained of weakness and

numbness in both legs and had some episodes of vagal experiences with

exertion. She described symptoms of dizziness and loss of memory,

light-headedness and vertigo, fatigue and a general cognitive

dysfunction. Four out 12 subjects had seen therapists in the past for

depression. Eight out of 12 complained of getting lost in a familiar

territory and had troubles getting words out at times and putting

their thoughts together. Initial clinical impression was subjective

memory dysfunction and possible aphasic symptoms without obvious

abnormality and pseudodementia.

In the year 2000, she moved into a home that was found to contain

abnormal levels of toxigenic molds that included: Aspergillus,

Stachybotrys, and Penicillium, and Cladiosporium genera. A private

environmental laboratory that used microscopic, culture, and chemical

techniques performed the toxigenic mold exposure characterization and

quantification. What was very unique about the patient was that all

the members of her family including their pet dog manifested similar

behavioral changes. On the advice of Insurance r and the

company that tested the home, she consequently moved out of her home

almost 2 months later. She was initially placed on Wellbutrin and

later she was tried on Topomax to which she complained of feeling

dizzy and so, stopped the medication. Although, she found a temporary

relief at that time, her major conditions persisted with increasing

loss of memory, neuropsychological problems, and allergic reactions.

The patient reported that she had marital difficulties and that the

family business where she worked was sold without her knowledge and

felt she did not have any meaningful occupational satisfaction. She

had sleep disturbances and was stressed out significantly as a

consequence. She reported being tested at the age of 30 for learning

disability. She had problems with muscular weakness, muscle and joint

ache, twitching muscles, painful lymph nodes and short of breath. It

was not inconceivable at that time she might have had mild cognitive

impairment associated with an early dementing illness or metabolic

encephalopathy. MRI investigation found herniated disc with no other

explanation, although, there was an indication of significant damage

to the parietal and frontal lobes of the brain.

MATERIALS AND METHODS

The patient was given comprehensive examinations to make sure that

their health conditions were fully evaluated. These examinations

included: the review of the patients' medical records, basic EEG

examinations including awake and asleep, photic stimulation, and

hyperventilation. Immunologic examination of the patient's blood

samples was done, using enzyme-linked immunoabsorbent assay (ELISA)

methods, Johanning et al., 1996). The psychological evaluation was

administered using a number of tests within the following cognitive

and neuropsychological domains (Wechsler1981; 1987; Rosenberg et al.,

2002): the Wechsler Adult Intelligence Test-III, Wechsler Memory

Scale, Luria-Nebraska Neuropsychological Battery, Trail making B Test,

Stroop Neuropsychological Test, Rey Auditory Memory Test, Mental

status Examination, Beck Depression Scale, the Minnesota multiphasic

personality inventory (MMPI), and Test of Proverbs. The reason for

the comprehensive test battery was to measure the intellectual

functioning yields (verbal), performance (nonverbal), and Full-Scale

IQ scores. The outcomes of these tests played a greater role in

ascertaining whether the patient's condition was due to an underlying

biogenic brain abnormality or attributable to the chronic toxigenic

mold exposures alone.

RESULTS

Immunologic examination: Most of the immunologic parameters, though,

outside the purpose of this paper, were abnormal. However, abnormal

IgG antibodies to Alternaria tenuis, Epicoccum nigrum, and Pullularia

pullulans antigens, but none of the toxigenic molds found indoor were

observed. Hence, there was no correlation between the toxigenic molds

found indoor with the abnormal antibodies to the three toxigenic mold

antigens found in the patient's serum (Table 1). IgG titers greater >

1600 found in the patient were suggestive of chronic exposure to all

the three fungi.

Table 1. Abnormal antibodies to Alternaria tenuis, Pullularia

pullulans, and Epicoccum nigrum mycotoxins mold antigens found in the

patient with neuropsychological impairments. Antibodies to all other

toxigenic molds were within normal values.

Test for antibodies

Abnormal values

ReferenceRange

IgG Alternaria tenuis

4800

0-1600

IgG Epicoccum nigrum

10600

0-1600

IgG Pullularia pullulans

2700

0-1600

Physiological examination: EEG examination showed 10 Hz posterior

dominant activities, which were synchronous, symmetrical and

attenuated on eye opening and eye-closure. Neither lateralized and

generalized background slowing, nor spike or sharp wave discharges

foci were identified. Also, hyperventilation did not alter the

background rhythm. Stage I sleep was recorded and the Awake EEG was

apparently normal. Her grip meter readings were L = 29; R = 30 and she

was unable to hold steady against the grid. There was an evidence of

tremor of the extremities. Her reflex was abnormal, and she had

accommodation paresis, arthralgia/joint pain, cough, fatigue,

headache, immune mechanism disorder, memory loss, mycosis, severe

muscular weakness, mood swing, intolerance to alcohol, personality

changes, anxiety, attention disturbances. She had speech disturbances,

frequently saying the wrong word, depression, dizziness, nausea, and

blurred vision.

Neuropsychological Evaluation:Summary of the patient's

neuropsychological performance is presented in Tables 2 and 3. Patient

had average intellectual abilities, which were about what could be

expected from her academic background and work role. Her working

memory on the intelligence test indicated a problem with short term

and immediate recall. Her memory score was significantly below other

index scores, and indicated some deterioration. Her processing speed

was her highest index score. Extreme anxiety and agitation was

observed throughout the tests. The Luria-Nebraska evaluation indicated

impairment in intellectual process, which reinforced the belief that

her general functioning was within that observed in the brain damaged

population and was significantly below non-brain damaged functioning.

Table 2: IQ measures for the patient with chronic exposures to

Alternaria tenuis, Pullularia pullulans, and Epicoccum nigrum

mycotoxins

IQ Measures

Scores

%

Verbal

101

53

Performance

104

61

Full-Scale score

102

55

Processing speed

108

70

Verbal comprehension

105

66

Perceptual Oriental

101

53

Lowest working memory

92

30

She indicated a general impairment, which demonstrated that she had

not compensated or adjusted appropriately for her cognitive

impairment. She demonstrated a probable arithmetic learning problem

and an indication of not being very academically oriented. There was

specific localization of injury found. Her memory quotient was 76,

which was extremely poor and indicated significant impairment. It was

significantly below her intellectual abilities in general. Her scores

on other memory tests were both good and poor and indicated an

intermittent lapse of memory rather than a consistent problem. She was

capable of learning given repetition. Hence, her impairment appeared

to be more attention and concentration oriented and thus might be more

of frontal, than temporal lobe of the brain in nature. However, she

indicated mild frontal lobe impairment primarily with attention,

concentration, mental agility and abstract reasoning. She appeared to

have a major depressive affective disorder of a moderate to severe

nature. She was agitated, with lagging attention and has unusual

beliefs that were unconventional. She presented with difficulty

concentrating and thinking. She had some unique somatic and bodily

delusions and was immobilized by multiple symptoms. She had chronic

relationship problems and was an underachiever for most of her life.

It seemed as though she was her own worst enemy. She presented with

some symptoms such as dizziness, light-headedness, which could be both

medical and psychological in nature. She presented with other anxiety

symptoms that gave credence to a functional diagnosis. Although it was

believed that she had an early dementia and major depression of

unknown etiology, pseudo-dementia was probably ruled out. Her weakness

and dizziness could also be a product of molecular encephalopathy.

Table 3:The summary of the neuropsychological findings in the patient

with chronic exposures to Alternaria tenuis, Pullularia pullulans, and

Epicoccum nigrum mycotoxins [(+++) = very high; (++) = high; (+) =

relatively low)].

Test Measures Overall Outcome Ranking

WAIS-III

Significant general impairment

+ + +

Luria-Nebraska

Intellectual process impairment

+ + +

MMPI

High level of impairment

+ + +

Stroop

Language impairment

+ +

Trait Making B Test

Multiple errors (70 sec)

+ + +

Beck Scale

Moderate depression

+ +

Test of Proverbs

Impaired abstract reasoning

+ + +

Behavioral observations:The patient presented as a cordial and

outgoing individual, well groomed, and appeared to be significantly

anxious with indications of mild to moderate depression. Her thought

processes appeared vague at times, and was high strung with agitation.

She indicated good cohesion between ideas and thoughts and her

judgment and decision-making appeared appropriate. There was an

indication of short term and immediate recall problems and she

appeared to have a concentration and attention deficit. She did not

make connection between her emotional state and physical symptoms and

appeared depressed with accompanying agitation and anxiety to warrant

a psychological diagnosis. She appeared somewhat " dazed " and

disconnected during some of the testing.

The patient was probably of average intellectual abilities and had

some difficulty with abstract reasoning and higher order thinking. Her

visual memory and perception was hampered with mild indication of word

loss. The patient may have a learning disability of a hyperactive

nature and appeared impulsive and easily distracted. There was an

indication of dyslexic behavior involving sequencing events in a

picture story right to left instead of left to right. The mini-mental

status examination yielded a mild to moderate problem thinking clearly

and reasoning in a rational fashion.

Intelligence tests: The WAIS-III indicated a verbal IQ of 101 at the

53%. Her performance IQ was 104 at the 61% and her full-scale score

was 102 at the 55%. There was no significant difference between the

verbal and performance scores. All scores were within the average

range of scores. Her highest index score was in processing speed at

108 and the 70%. Verbal comprehension was 105 at the 66%, perceptual

oriental was 101 at 53% and the lowest was working memory at 92 and

the 30%. Her working memory was significantly lower than other index

scores and indicates a problem with short term and immediate recall.

The working memory score is significantly below other index scores.

The average scaled score is 10. The patient scored 103 on verbal and

10.6 on performance. Both scores are at or slightly above the national

average. Her IQ scores are about what could be expected given her

academic background and occupational track.

Intellectual processes: The patient indicated her scores discriminate

between brain damaged and non-brain damaged individuals. Generally her

score fell within the brain damaged category. It is heavily influenced

by left hemisphere activity. She generally performed below those

without brain damage. However, her performance supported the MRI

observation of a possible damage to the parietal lobe or frontal lobe

of the brain.

Working memory: The Wechsler Memory Scales indicated a memory quotient

of 76. This is extremely poor and indicates a score within the

borderline category. This score is significantly below her

intellectual abilities and thus indicates a cognitive impairment. She

indicates problems with mental control, logical memory, digit span,

and visual memory. The Rey Verbal Learning Test indicated no

impairment in auditory learning. Her scores were all average in

immediate and short-term verbal recall. Her digits span scores

indicated a problem with attention and concentration. Her short term

and immediate recall was appropriate. Her letter-number score on the

WAIS was significantly above the norm. This is both an immediate

recall and attention measure. The patient indicated significant

intermittent problems with short-term memory and in particular

attention and concentration. She does perform significantly better

with repetition and thus is capable of learning new material with

repetition. She indicated significant attention and concentration

difficulties.

Frontal lobe and executive functioning: The Trail making B Test

indicated multiple errors involving mental agility and planning. Her

score of 70 seconds indicated a minimal impairment and confusion

involving right hemisphere activity. The Stroop test indicated no

impairment of a language nature involving mental agility. This was a

left hemisphere task. The similarities score on the WAIS indicated a

score above the national average. The matrix reasoning score was

slightly above the national average. There was an indication of

attention and concentration problem. The Test of Proverbs indicated a

mild impairment in abstract reasoning. She indicated a mild impairment

of the frontal lobe primarily with attention and concentration, mental

agility and abstract reasoning.

Personality:The Beck Scale indicated moderately depressed individual.

She felt sad, discouraged and had a sense of failure. She did not

enjoy things like she used to and had become annoyed and irritated

much more easily. Her decision-making skills had suffered and she got

tired much more easily now. She lacked a drive and motivation. She

indicated some feelings of dizziness and light-headedness frequently.

She was jumpy and had a fear of dying. She felt a weakness and was

unable to relax. She was highly nervous. The MMPI indicated a

significant psychological disorder in the form of agitation, lagging

attention in the midst of crisis. She has unusual beliefs and is

alienated and unconventional. She had identity confusion and had

difficulty with concentration and thinking. She overemphasized

pathology and was cynical. She possessed some unique bodily or somatic

delusions and was immobilized by multiple symptoms. She had problems

with authority and might have had recurrent work and family problems.

She had a history of underachievement and relationship problems. She

probably was insecure, anxious, a worrier and was indecisive. She was

an exhibitionist. Her behavior appeared to be functional or

psychological in nature rather than attributed to primary organic

concerns.

Treatment: Treatment of mycosis in general is a serious challenge to

health care personnel and requires the understanding of the basic

pathophysiological mechanisms that underlie their drug resistance. In

some patients, the symptomology is more persistent due to patient

susceptibility, fungal growth patterns that resist treatment and the

occurrence of dormant fungal spores. Although new antimycotic agents

are far more promising than the ones used in earlier treatments,

relapse rates still remain high. Treatment can include systemic

antifungal therapies as well as nonpharmaceutical methods. A number of

modern treatment strategies are available and are generally well

tolerated and effective. However, the MedicalCenter for Immune and

Toxic Disorders devised a systematic treatment approach that takes

into account the sensitivity of drug to fungal organism,

adverse-effects profile, dosage schedule, and duration of therapy,

concomitant medical conditions, and concurrent medications (,

2001). Nevertheless, complete treatment will depend on several

factors, including appropriate spectrum of activity, adverse effects,

and potential drug interactions plus patient preferences for specific

dosing regimens.

DISCUSSION

Considering the findings in this patient's test analyses, it appeared

that three major complex factors might have played a role in her

clinical conditions. First, the patient's indoor environment was

contaminated with toxigenic molds that were different from those found

in her serum. Secondly, there were three toxigenic molds found in the

patient's serum to which the synergistic contribution of each

toxigenic mold to the patient's psychological condition was difficult

to ascertain. Thirdly, the patient had significant traumatic

experiences involving her work and marriage, each of which was capable

of exerting psychological influence on her well being. The question

then is, which of these factors was responsible for the patient's

condition? The first factor is ruled out completely, since there was

no relationship between the toxigenic mold contamination of the indoor

environment, and the toxigenic mold antigens found in the patient's

serum. Therefore, the last two factors are most likely responsible for

the patient's condition, but the time and sequence of cause-effect is

difficult to say without a proper analysis of individual likelihood of

exerting psychological effects. Consequently, we looked in depth, at

the abnormal antibodies to three toxigenic mold antigens found in the

patient's serum to identify the most likely species that might have

exerted the most psychological effects on the patient.

Mycotoxins produced by Alternaria tenuis: Alternaria tenuis occurring

in isolates from tomato, and polished rice produces tenuazonic acid

mycotoxin with two isomeric forms namely: standard tenuazonic acid and

isotenuazonic acid. Some species of toxigenic Alternaria tenuis

produce alternariol (AOH), alternariol methyl ether (AME) (Bjeldanes

et al., 1978), and tenuazonic acid mycotoxins, and it was shown that

small amounts of tenuazonic acid have pronounced mutagenic activity

(Bjeldanes et al., 1978; and Kanhere, 1980).

Pullularia pullulans lack mutagenic and or carcinogenic potential,

therefore, lack significant toxicological activity (Velcosvsky and

Graubner, 1981; Tarabasz-Szymanska and Galas, 1993; Kimoto et al.,

1997), even though, acute exogenous allergic alveolitis with the

typical symptoms of unproductive cough, dyspnoea on exertion, fever,

weight loss, headache, and limb pains was observed in a 24-year-old

bank employee. Also, pullulans have been implicated in leucocytosis,

hypoxemia, and marked restrictive ventilatory defects (Velcosvsky and

Graubner, 1981). Kimoto et al. (1997) found no indications of an

adverse effect of pullulans on hematology and clinical chemistry

values of treated animals and there was no indication of

pullulan-related toxicity in terminal organ and body weights.

Epicoccum nigrum synthesizes extracellular fungal polysaccharide,

called epiglucan (Schmidt et al., 2001). The Epicoccum nigrum extracts

used in allergy disorders exhibit batch-to-batch variations in protein

composition and allergenic potency (Bisht et al., 2000). Ambivalently,

Epicoccum nigrum (EN) was obtained consistently from four patients who

were having allergic fungal sinusitis (AFS), indicating that E. nigrum

can colonize nasal sinuses and cause AFS (Schmidt et al., 2001), and

that EN is a significant allergen in urban communities (Dixit et al.,

1992; Schmidt et al., 2001). However, Epicoccum nigrum has antibiotic

properties (e.g., epicorazine A), hence, was found to exhibit an

activity against Staphylococcus aureus (Baute et al., 1978; Deffieux

et al., 1978; Deffieux et al., 1978).

Which toxigenic mold was responsible for the patient's health

condition? The question here is, which toxigenic mold antigen was

responsible for the patient's condition? It is rather difficult to say

with greater confidence without further experimental evaluation of the

physiological and toxicological effects of these antigens. However,

from the background literature that was stated thus far, it appeared

that each of these antigens must have contributed in different

measures, to the patient's conditions. Considering the structural and

functional groups in the metabolites of the three toxigenic molds, one

would suggest that Alternaria tenuis probably has the most damaging

effects since it exhibits mutagenicity and carcinogenicity. Pullularia

pullulans, on the other hand, no such effects besides allergenicity,

which was the patient's main health problem. Epicoccum negrum produces

metabolites that are more of antibiotics than mycotoxins. Therefore,

it is more likely that Alternaria tenuis may have major contributory

psychological effects than the other two toxigenic molds.

Relationship between patient's physical experience and toxigenic

molds: It is true that the human brain has the ability to maintain its

normal function even when the mind is placed under a severe physical

pain. However, if the brain is anatomically damaged, such an endowment

is compromised and the individual becomes susceptible to psychological

changes. It is possible therefore that the time sequence of events

that led to the patient's psychological conditions probably began with

the chronic toxigenic mold antigens in the serum that in turn, led to

the changes in the brain structure consequent upon which the mind and

behavior were affected.

Conclusion: In several cases reported in the literature, it was often

obvious to observe an association between indoor environmental

toxigenic mold exposures with the patients' relevant seromycological

positives. However, this " axiom " is not always true because, as we

have found in this case, the identity of the abnormal levels of

toxigenic molds observed in the indoor environment were different from

those observed immunologically in the patient's blood. Clinical

neuropsychological impairments associated with chronic exposures to

those toxigenic molds (Alternaria tenuis, Pullularia pullulans, and

Epicoccum nigrum) have been reportned. The overall findings seemed

support the views that certain toxigenic molds are particularly a risk

factor for adverse human health, including neuropsychological

disorders. In addition, abnormal antibodies to toxigenic molds in the

serum of the patients may reflect the adverse health conditions

synergistically, however, only one abnormal antibody to toxigenic mold

antigen could have the most adverse toxicity leading to

neuropsychological effects. It is concluded therefore, that although,

it is acknowledged that the contamination of the indoor environment by

toxigenic molds directly related to adverse the health effects on the

occupants, however, there could be a situation where such relationship

does not exist. Here, we have reported such a situation.

Acknowledgement:

We are grateful to the MedicalCenter for Immune and Toxic Disorders,

Spring, Texas, USA.

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