p. 1 

GRAND ROUNDS 

in Environmental Medicine 

CHILDREN'S MERCY HOSPITAL 

Infant Pulmonary Hemorrhage in a Suburban Home with Water Damage and 

Mold I Stachybotrys atral 

Susan M. Flappan, Jay Portnoy, Patricia Jones, and Charles Barnes 

Department of Allergy, Asthma, and Immunology, Children's Mercy Hospital, Kansas City, Missouri, USA 

The American Academy of Pediatrics recently issued guidelines regarding the potential toxic 

effect of indoor molds. We now report another case of an infant with pulmonary hemorrhage 

whose residential environmental assessment revealed the presence of the toxigenic mold 

Stacbybotrys atra. We used a questionnaire to identify environmental factors that could predispose the home to fungal contamination. We collected air samples from multiple locations in the 

home that we felt would reflect areas of relevant exposure . Surface samples were collected with a 

piece of transparent tape for serniquantitative measurement of spores present. We classified spores 

into their respective genera based on shape, size, and color. We also measured mycotoxin levels. 

Air sampling revealed significantly elevated total spore counts in the patient's bedroom and in the 

attic. Aspergillusl Peniieillium species were predominant. Stacbybotrys spores were found in the air 

sampled in the patient's bedroom, as well as from surfaces sampled in the patient's closet and the 

attic ceiling. Additionally, a small patch of Stacbybotrys-contaminated area in the closet ceiling 

was sent for mycotoxin analysis . This material proved to be highly toxigenic. As the link between 

the presence of Stachyboay, in the home and pulmonary hemorrhage in infants increases, further 

efforts should be made to educate physicians, health care providers, and new parents about the 

potential toxic effects of this mold . Key word;: floods, fungus, idiopathic pulmonary hemorrhage, 

IPH, mold exposure, mycotoxins, Stachybotrys, toxic mold, tricothecenes, water damage . Envirare 

Health Perspect 107:927-930 (1999) . [Online 20 October 19991 

bttpa/ehpnetl .niebs.nib.gov/docsl1999/107p927-930flappan/abstract.btnnl 

Pulmonary hemorrhage is a relatively infrequent condition in infants that can result in 

significant morbidity and mortality (1) . Its 

diagnosis is based on the identification of 

alveolar hemosiderin-laden macrophages 

(iron-staining white cells) from bronchoalveolarlavage or biopsy . A cluster of 10 cases of 

idiopathic pulmonary hemorrhaging (IPH) 

occurred during 1993 and 1994 at Rainbow 

Babies and Children's Hospital in Cleveland, 

Ohio. In the decade preceding these years, 

there had been only 3 cases of IPH at the 

same hospital (1) . An examination of the circumstances that may have lead to pulmonary 

hemorrhage in these infants suggested a link 

between IPH and water damage in the 

patients' homes. Higher exposures to fungi, 

and particularly to Stachybotrys atra, were 

found in case homes versus control homes. 

(3) Ninety percent of the patients in the 

study were also exposed to tobacco smoke. 

The residences were an average of 75 years 

old and most were in poor repair, suggesting 

that socioeconomic factors may predispose 

patients to this type of fungal exposure. (4) . 

We now report another case of pulmonary hemorrhage in an infant who resided 

in a newer, middle-class home located in the 

suburbs . Environmental testing of the residence was conducted a few days after the 

child was hospitalized. This allowed evaluation of the home at nearly identical conditions as those present before the patient's 

hospitalization. 

Case Presentation 

A 1-month-old infant presented to the emergency department at Children's Mercy 

Hospital, Kansas City, Missouri, with acute 

onset of respiratory distress and shock. He 

was a hill-term, healthy baby at birth and had 

had no prior symptoms preceding this sudden illness . That morning he had vomited at 

home, became very fttssy, and was difficult to 

console . By the afternoon he was breathing 

rapidly and was grunting. On arrival at the 

hospital he was pale and cyanotic. He had 

developed nasal flaring and intercostal retractions. He had a blood pressure of 57/17 and 

a rectal temperature of 36.3°C . He was also 

lethargic and nonresponsive to pain. His 

extremities were cool and mottled. 

The patient's condition deteriorated over 

the next 30 min. Due to progressive respiratory distress, an endotracheal tube was inserted 

without trauma . A moderate amount of bright 

red blood was suctioned from the tracheal 

tube immediately after insertion and several 

times thereafter . Bronchoalveolar lavage 

demonstrated that 2% of the macrophages 

contained iron-positive material, an indication 

of hemosiderosis (white blood cells engulfing 

red blood cells) . Hemosiderosis indicates longterm bleeding and does not result from an 

acute episode of pulmonary hemorrhaging (25 . 

Other laboratory test results showed an 

elevated white blood cell count (30,400/m3) 

with no left shift, a decreased hemoglobin 

and hematocrit (10 .1 g/dL and 29.3, respectively) ; an elevated prothrombin time (17 .7 

sec; normal 10-14.3 sec) ; and an elevated 

platelet count of 457,000/dL. Bacterial cultures collected from the blood, urine, cerebrospinal fluid, and tracheal aspirate were all 

negative. This made a diagnosis of disseminated intravascular coagulation due to septicemia very unlikely. Viral cultures of the 

nasopharynx and rectum were also negative. 

A supine chest radiograph showed diffuse 

bilateral alveolar densities throughout the 

lungs with no pleural effusions or pneumothorax. Milk-specific IgE was negative . 

Because the attending physician was 

aware of the information relating pulmonary 

hemorrhage to fungal exposure (5), the environmental health specialist from the allergy 

section was requested to assess the patient's 

home for Stachybotrys. Supportive care was 

provided and the infant recovered ; he subsequently was discharged to live in his maternal grandparents' home until the paternal 

grandparents could address environmental 

concerns raised by this investigation. 

Address correspondence to S.M. Flappan, 

Children's Mercy Hospital, Department of Allergy 

and Immunology, 2401 Gillham, Kansas City, MO 

64108 USA. Telephone: (816) 234-3097 . Fax: 

(816) 346-1301 . E-mail : Sllappan@cmh.edu 

The authors thank K. Wible and M. Sheffield, 

Children's Mercy Hospital; B. Jarvis, University of 

Maryland ; D. Dearborn, RB& C Hospital, 

Cleveland, Ohio; and R. Etzel, American Academy 

of Pediatrics for their assistance . 

This study was supported by Children's Mercy 

Hospital ; KB Richardson Fund . 

Received 19 July 1999 ; accepted 27 August 1999 . Environmental Health Perspectives " Volume 107, Number 11, November 1999 927 
Grand Rounds in Environmental Medicine " Flappan et al . 

Methods 

A home visit by a certified industrial 

hygienist was performed 4 days after the 

infant presented to the emergency department. During that visit, responses of family 

members to a questionnaire were used to 

identify potential environmental factors 

that could predispose the home to fungal 

contamination . 

Air samples were obtained using an 

Allergenco MK-3 volumetric spore trap 

(Allergenco/Blewstone Press, San Antonio, 

TX) (Figure 1) . The device was set to collect 

10-min air samples at 15 L/min in the 

infant's bedroom, the bedroom closet, the 

attic space above the closet, the family room, 

and the kitchen . We considered these locations to be relevant to the patient's exposure . 

We collected the samples during a cold period in the winter when the outdoor mold 

count was negligible . The Allergenco MK-3 

drew airborne particles through a small opening (1 .1 x 14.5 mm) in its lid . Particles 

impacted onto a grease-coated slide positioned in a slide carrier underneath the opening . A line of particle deposition formed 

called a trace . After each sampling period, the 

slide carrier automatically advanced to a new 

positon to allow a new trace to form. Thus, 

each trace represented a room or location 

sampled. The slide was stained with 

Calberla's (6) in the laboratory and read 

microscopically at 1000x magnification . 

Counts per cubic meter were calculated based 

on the number of spores observed in five horizontal sweeps of a trace . 

We collected surface samples with transparent cellophane tape (tape prep) for 

semiquantitative measurement of mold contamination. All spores were classified into 

their respective genera based on shape, size, 

and color . 

Results 

The infant's exposure occurred at the paternal grandparents' house where he shared a 

small bedroom with his mother. Water 

damage to the house occurred when shingles 

on the roof, which had recently been 

replaced and improperly installed, were 

damaged during a hail storm. This allowed 

rainwater to enter the attic and the baby's 

bedroom closet located directly below the 

leak . As a consequence, fungal contamination developed on the attic ceiling and in 

the closet (Figure 2) . 

Airborne spore counts were taken in the 

five locations shown in Table 1 . Stachybotrys 

spores were observed in the air collected 

from the infant's bedroom . Four surface 

samples taken from water-damaged building 

materials also contained Stacbybotrys spores: 

one from the closet ceiling, one from the 

closet door, and two from black stains on the 

attic ceiling . Several other microbials were 

also identified from visually contaminated 

sites including AspergilluslPenicillium, 

Memnoniella, Alternaria, ascospores, 

Cladosporium, Chaetomium, Torula, and 

bacterial bacilli. 

We collected additional surface samples 

of dust in the infant's bedroom to determine the extent of spore migration from the 

original sites of colonization . One sample 

taken from the bedroom supply vent contained a moderate amount of Stachybotrys. 

Stachybotrys was also present in dust from 

the infant's crib and mattress (after the 

sheets had been removed) . Other surface 

samples from the room fan (free-standing, 

portable electric fan), the miniblinds, and 

the television contained an assortment of 

fungal spores including Cladosporium, 

Periconia, ascospores, AspergilluslPenicillium, 

Chaetomium, Alternaria, and Myxomycetes 

species, but no Stacbybotrys was observed. A 

tape prep collected from the washable electrostatic furnace filter was heavily contaminated with Aspergillus/Penicillium species, 

and also a rare Stacbybotrys spore was 

observed . The detection of Stachybotrys on 

the furnace filter indicated that these spores 

had entered into the ventilation system . The 

Stachybotrys spores could be distributed to 

other parts of the home via the ductwork 

unless the furnace filter captured them from 

the circulating air . 

We used a sterile swab to collect samples 

for culture from a small area of closet wallboard where Aspergillus/Penicillium species 

had been detected . This swab was then inoculated onto blood and malt extract agar and 

incubated at room temperature . Our goal 

was to further differentiate the Penicilliuml 

Aspergillus genera into more specific classifications. We observed growth of two types of 

Penicillium species, gram-negative rods, and 

Rbodotorula yeast . 

To determine if the Stacbybotrys spores 

were toxigenic, we removed a 10-cmz area of 

contaminated closet ceiling after thoroughly 

wetting it down to prevent aerosolization of 

spores . This specimen was sealed in a bag 

and shipped to Bruce Jarvis at the University 

of Maryland for mycotoxin analysis by 

HPLC. High quantities of several potent tricothecenes were detected in this sample . The 

mycotoxins Roridin L-2, Roridin E, and 

Satratoxin H were measured at levels of 0.5, 

0.7, and 3.2 ng/cm2, respectively. 

Environmental Remediation 

Our primary recommendation was that the 

cause of water entry, the leak in the roof, 

should be repaired. We also suggested that 

visible mold and mold-contaminated items 

should be disinfected and/or removed in 

accordance with the Stachybotrys remediation 

guidelines written by the New York City 

Department of Health (A A third suggestion was that the family should filter, clean, 

vacuum, and dust all surfaces and items 

which might contain migrant spores, including the ventilation system. We strongly 

advised this family to prevent the infant from 

entering the contaminated home until the 

cleanup was complete because many infants 

diagnosed with Stachybotrys-associated pulmonary hemorrhage continue to have hemosiderosis for up to 6 months after hospital 

release (2) . We also emphasized that the 

infant should not be exposed to environments contaminated with tobacco smoke. 

Ideally, a follow-up survey should be done to 

confirm that fungal contamination has been 

Rgure 1 . Photograph of the Allergenco MK-3 air 

sampler (Allergenco/Blewstone Press, San 

Antonio, TX). Airborne particulates drawn through 

a small opening (1 .1 x 14 .5 mm) in the lid impact 

onto a microscope slide underneath. Both viable 

and nonviable spores are detected by direct 

microscopy . 

Fgure 2 Photographs of the (A) ceiling and (8) floor of the closet in the child's bedroom. Stains indicate 

water damage from rain entry. Stachybotrys mold growth was found; other microbials were also present, 

including Chaetomium, Cladosporium, and AspergillusJPenicillium mold spores; Rhodotorula yeast and 

gram-negative bacteria. 

928 Volume 107, Number 11, November 1999 " Environmental Health Perspectives 
Grand Rounds in Environmental Medicine " Infant pulmonary hemorrhage and stachybotrys 

resolved before an infant returns to an affected environment. Because this family elected 

to have the infant move to a different home, 

follow-up measurements were not performed. Although the threat of IPH appears 

to decline after 1 year of age (8), it is still 

preferable for the infant to avoid mold and 

smoke-contaminated environments after 

that time . 

Discussion 

To determine if the Cleveland duster of 10 

IPH cases during 1993 and 1994 was related 

to environmental exposures, the Centers for 

Disease Control and Prevention (CDC) conducted a case-control study (4) . In that 

study, the Cleveland cases were matched with 

30 controls having similar zip codes (lived in 

similar areas) and ages . Air and surface samples from rooms where the infants spent the 

most time were collected and analyzed. Mean 

total spore and Starhybotrys atra spore counts 

from air samples were found to be significantly elevated in case homes as compared to 

control homes. Surface samples in case versus 

control homes also had much higher concentrations of Stachybotrys spores . Etzel et al . (4) 

concluded that infants who experienced pulmonary hemorrhaging and hemosiderosis 

were 16 times more likely than controls to 

have lived in homes with water damage due 

to roof leaks, plumbing leaks, or flooding . 

The authors identified no differences 

between cases and controls with regard to 

pesticide exposure, infant products used, or 

cocaine use of family members. Exposure to 

tobacco smoke increased the odds of pulmonary hemorrhaging by 8-fold (4) . 

There are a number of similarities 

between the Cleveland cluster of IPH cases 

(4,9) and the case study reported here . Our 

patient lived in a home with water damage, in 

this case due to a roof leak . In both the 

Cleveland homes and this case study, mold 

damage had not been cleaned up before environmental testing, although there was a 

longer time interval in Cleveland between 

occurrence of hemorrhage and the environmental survey. As in the Cleveland duster of 

case homes, this home had elevated levels of 

airborne spores, with the highest concentration found in the patient's bedroom. 

Airborne Stacbybotrys was among the spores 

detected. As was true for the Cleveland 

homes, the patient's home revealed significant 

amounts of Stachybotrys from surface samples. 

In both instances, several other microbials 

were present in addition to Stachybotry, raising the question of whether IPH may be 

caused by interactive or synergistic effects of a 

combination of biocontaminants and/or their 

metabolites (9~ . Mycotoxin analysis of the 

Stachybotrys-contaminated plaster from the 

closet ceiling in this case showed a high level 

Table 1 . Air sample spore counts per cubic meter by genus in five different rooms . 

Patient's Closet of 

bedroom bedroom 

Attic above Family 

bedroom room Kitchen 

Total spores/m3 13,440 4,368 

A/P sp . 11,256 4,032 

Cladosporium 1,512 252 

Altemaria 0 0 

Ascospores 168 84 

Periconia 84 0 

Chaetomium 0 84 

Stachybotrys 420 0 

2,856 2,520 1,512 

2,352 2,184 1,092 

336 252 168 

84 84 0 

84 84 84 

0 0 0 

0 0 0 

0 0 0 

A/P sp ., AspergilluslPenicillium species. 

of toxicity, as was true of isolates taken from 

air and surface samples in the Cleveland 

homes (1U) . 

Additional similarities between the 

Cleveland cluster of cases and this reported 

case include a) the ages of the infants (4-16 

weeks); b) bottle-feeding infants a cow's 

milk-based formula ; c) tobacco smoking by 

the parents, d) red blood cell profiles consistent with normochromic, normocytic anemia; e) chest X rays showing diffuse bilateral 

infiltration consistent with pulmonary hemorrhaging; and f ) no other sources of bleeding. Microbiology cultures of the blood, 

urine, and bronchoalveolar lavage from 

almost all of the Cleveland infants were 

negative for bacterial, fungal, and viral 

pathogens, as was true for this case (4) . The 

majority of Cleveland infants had signs of 

respiratory failure before signs of internal 

pulmonary bleeding became apparent (2'), as 

happened in our case study. 

There are also some important differences between our patient and those in the 

Cleveland duster . The 10 infants in Cleveland 

were all African American and lived in an 

inner-city area . Their residences were an 

average of 75 years old and many were in 

poor repair (4) . In contrast, our infant was 

white and he lived in a 15-year-old suburban 

home that was in relatively good repair . 

Water damage to our patient's home was a 

result of faulty workmanship, not because of 

neglect. This demonstrates that water contamination with resultant Stacbybotrys contamination can occur in any type of home and 

that it is not a condition limited to the inner 

city. A moisture problem that is not properly 

cleaned up in a reasonable amount of time 

can lead to indoor mold growth regardless of 

the home's age or location . 

Stachybotrys atra is a fungus that originates in soil and plant debris, and it has a 

wide geographic distribution . To grow in 

indoor environments, Stacbybotrys requires 

long-term water saturation of cellulose-based 

material such as paper, cardboard, wood, 

plasterboard (wallboard), or jute-backed carpet . Plumbing leaks, roof leaks, or rainwater 

flooding into basements can provide the 

needed moisture for this mold to thrive . 

Stachybotrys spores are sticky while still moist, 

but the fungus becomes powdery when the 

substrate dries out. The spores can become 

aerosolized if disturbed (Z) . Their small size 

and ellipsoid shape allow them to be inhaled 

and to reach the lower respiratory tract 

(Figure 3) (2,11) . 

Stacbybotrys was first associated with a 

toxic response in animals in Eastern Europe 

and the Ukraine in the 1930s. Horses consuming contaminated straw or hay showed 

shock, dermal necrosis, leukopenia, nervous 

disorders, and death. This condition was 

later termed stachybotryotoxicosis . Since 

then, similar problems have been reported 

throughout the world, primarily in Eastern 

Europe (12) . 

The first reported cases of stachybotrytoxicosis in people occurred in the 1940s. 

Russians who handled tainted hay or slept 

on straw-filled mattresses experienced dermatitis, pain, and inflammation of the 

mucous membranes; burning nasal passages ; 

tightness of chest ; bloody rhinitis ; cough; 

fever ; headache; and fatigue (125 . 

From the 1950s to the 1980s, more 

papers were published on the topic, but few 

reports identified Stachybotrys in homes or 

buildings . In 1986, Croft et al . (1A reported 

an outbreak of mycotoxicosis in a Chicago 

home with chronic moisture problems . 

Extracts of mold-contaminated materials 

from this residence were shown to be highly 

toxic to test animals. After the mold problems had been corrected, the multisystem 

symptoms (headaches, sore throats, hair loss, 

flu symptoms, diarrhea, fatigue, dermatitis, 

severe leg pains, malaise, and depression) of 

the family resolved (1A. 

There have been other reports regarding 

the relationship between Stacbybotrys and 

health effects to humans. In a controlled 

study, Johanning et al . (14) compared 

chronically exposed office workers to nonexposed office workers . Significant differences 

were found between exposed employees (n = 

53) and controls (n = 21) in regard to lower 

respiratory, dermatologic, eye, chronic 

fatigue, and immune system symptoms (14) . 

Many studies have demonstrated that 

Stachybotrys atra is capable of producing 

Environmental Health Perspectives " Volume 107, Number 11, November 1999 929 
Grand Rounds in Environmental Medicine a Flappan et al . 

to pm 

Figure 3. Stachybotrys spores (at 1000x magnification) are ellipsoid in shape, are 4-6 pm x 1-12 

pm in size, and have an aerodynamic diameter of 

5 pm (10) . Particles with aerodynamic diameters 

< 7 pin can have appreciable (> 9%) alveolar 

deposition (11). 

potent tricothecene mycotoxins (10,12-17) . 

These include the macrocydic tricothecenes 

Roridin E, Roridin L-2, Satratoxin H, and 

Satratoxin G, all of which are potent protein 

synthesis inhibitors and highly cytotoxic to 

eukaryotic cells . Experimental laboratory 

animals have shown physiologic effects similar to those observed in farm animals with 

stachybotrytoxicosis . Tricothecenes are 

thought to be the primary reason for the 

health problems. Stacbybotrys spores are also 

capable of producing spirolactones, spirolactams, and cyclosporin, mycotoxins with 

immunosuppresant effects (10) . Infants may 

be especially susceptible to the effects of 

spore-borne mycotoxins due to their high 

breathing rate, immature lungs, and rapid 

growth. Exposure to tobacco smoke may 

serve to augment overt expression of pulmonary bleeding. 

A question that remains to be answered 

is how exposure to Stacbybotrys can lead to 

IPH or other health symptoms if so few 

spores are actually airborne. A number of 

possibilities have been suggested, including 

the presence of antigens or mycotoxins in 

the air that are not associated with intact 

spores, volatile organics, or high numbers of 

spores dispersed intermittently . The latter 

possibility, that spores were dispersed intermittently, is supported in this case study 

because there was an electric fan in our 

patient's bedroom. Fans may promote 

greater dispersal of spores, making them 

available for inhalation and human contact. 

Over 87% of the Cleveland cases also had 

electric room fans (~. 

Conclusion 

From 1993 to 1998, a total of 37 cases of 

IPH were found in the Cleveland area. 

Twelve of these infants died. Another 138 

cases have been reported to the CDC from 

all over the country in that same period (2) . 

In June 1998 the American Academy of 

Pediatrics (AAP) published an article warning that infants under 1 year of age should 

not be exposed to chronically mold-contaminated indoor environments (S) . The AAP 

recommended that if an infant presents with 

symptoms of IPH, parents should be questioned about water damage in the home. 

The AAP recommended that if an infant 

dies suddenly from an unknown cause, an 

autopsy that includes Prussian blue staining 

of lung tissue should be performed to check 

for hemosiderin-laden macrophages (5) . 

With these recent AAP recommendations, the medical community has become 

more aware of the association between exposure to Stachybotrys mold and the incidence 

of IPH. However, cause and effect have yet 

to be firmly established . As more cases of 

IPH are documented throughout the country, the correlation with Stachybotrys exposure may be strengthened . It is important 

that this information be passed on to the 

general public in a timely manner, with special emphasis given to parents of young 

infants, physicians, and hospital personnel . 

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930 Volume 107, Number 11, November 1999 " Environmental Health Perspectives