Chronic Environmental exposure to Alternaria tenuis may manifest symptoms of neu

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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 and Environmental Management World Bank assisted

National Agricultural Research Project (NARP) - University of Port Harcourt

ISSN: 1119-8362 Vol. 9, Num. 3, 2005, pp. 45-51

 

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

3, 2005, pp. 45-51

 

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 riskâ€

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 Carrier 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 (Evans, 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;

Scott 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 “axiomâ€

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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