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Implications of Detecting the Mold Syncephalastrum in Clinical Specimens of New Orleans Residents After Hurricanes Katrina and Rita

Rao, Carol Y. ScD; Kurukularatne, Changa MD; Garcia-Diaz, Julia B. MD; Kemmerly, Sandra A. MD; Reed, Deoine PhD; Fridkin, Scott K. MD; Morgan, Juliette MD

Journal of Occupational & Environmental Medicine: April 2007 - Volume 49 - Issue 4 - pp 411-416
doi: 10.1097/JOM.0b013e31803b94f9
Original Articles

After the extensive flooding in New Orleans following Hurricanes Katrina and Rita, thousands of homes in the flooded areas had significant growth of mold. The potential health effects from exposures to these extraordinary environments are unknown. In February 2006, we investigated a cluster of patients with clinical specimens yielding Syncephalastrum, a zygomycete that rarely causes infection. We identified the cases of eight patients from September 12, 2005, to January 12, 2006, with specimens from sputum, bronchoalveolar lavage, endotracheal aspirate, ear swab, and nasal swab. All patients appeared to be transiently colonized without evidence of infection, even among immunosuppressed patients. Only one patient reported significant exposure to mold (working on mold remediation without wearing a respirator) on the day of his incident culture.

From the Epidemic Intelligence Service (Dr Rao), and Mycotic Diseases Branch (Drs Rao, Fridkin, and Morgan), Centers for Disease Control and Prevention, Atlanta, GA; and the Ochsner Clinic Foundation (Drs Kurukularatne, Garcia-Diaz, Kemmerly, and Reed), New Orleans, LA.

Address correspondence to: Carol Y. Rao, ScD, Centers for Disease Control and Prevention, 1600 Clifton Road, MS C-09, Atlanta, GA 30333; E-mail: Cnr3@cdc.gov.

After Hurricane Katrina’s landfall on the Gulf Coast on August 29, 2005, several breaches occurred in the levee system in New Orleans, Louisiana (NOLA). As a result, large areas of NOLA were flooded for several weeks, providing optimal conditions for mold growth in buildings. Since early October 2005, evacuated residents gradually started returning to the city. Many returning residents did not consistently use appropriate personal protective precautions while in their moldy homes.1 Although no airborne mold concentration limits to prevent illness have been defined, there was great concern for the potential health effects from exposures to these extraordinary conditions, especially among those at higher risk of developing illnesses from exposures to molds (eg, the immunocompromised, people with asthma).2,3

In January 2006, the Ochsner Clinic Foundation (OCF) reported isolating Syncephalastrum in several post-hurricane clinical specimens. Only six cases of people with Syncephalastrum infections have been reported in the literature.4–9 The source of the mold for these individuals was thought to be from exposures to water-damaged buildings after the hurricanes. Syncephalastrum, a zygomycete, is an environmental mold that grows well on wet substrates. Although Syncephalastrum is found in soil and animal dung in tropical and subtropical regions, it has rarely been found in the air in the Southeastern United States (<1% of 706 buildings) prior to Hurricanes Katrina and Rita.10,11 In October 2005, however, thermotolerant airborne Syncephalastrum was recovered in 47% of the heavily damaged and moldy NOLA houses sampled and in none of the mildly damaged NOLA houses.12 We investigated the implications of isolating an environmental mold in clinical specimens and the nature of the exposures to mold.

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Materials and Methods

Case Ascertainment and Definitions

We defined a case as a positive culture result for Syncephalastrum from any clinical specimen obtained between September 1, 2005, and February 28, 2006 (the investigation period), from a resident of greater NOLA. Cases were classified into the following categories: confirmed invasive disease (symptoms compatible with an invasive mold infection, and histological evidence of tissue invasion), possible invasive disease (symptoms compatible with an invasive mold infection without another likely etiology and responded clinically to treatment appropriate for zygomycetes), colonized (no symptoms compatible with an invasive mold infection or had compatible symptoms with another likely etiology, and resolved without treatment appropriate for zygomycetes).

We conducted case findings by reviewing microbiology laboratory records for Syncephalastrum isolated for all clinical specimens obtained during the investigation period. If available, tissue and bronchoalveolar lavage (BAL) specimens were stained and examined under direct microscopic examination for fungal elements. We conducted a detailed review of the medical records and abstracted relevant clinical and demographic data on the cases.

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Evaluation of Exposure

For each case, we administered a standardized questionnaire to evaluate and characterize the patients’ exposures to moldy indoor environments after Hurricanes Katrina and Rita. If the patient was incapacitated, a close relative was then interviewed.

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Laboratory Investigation

We assessed microbiology laboratory standard operating procedures for the analysis and identification of molds in clinical specimens. We obtained data regarding the daily total number of ear, nose, and throat (ENT) and respiratory clinical specimens submitted for culture (either for routine culture or fungal culture) during the period of investigation. In addition, we reviewed any reported Syncephalastrum isolated from clinical specimens dating back to January 1, 2004. We reviewed the log-in records for the date, time, and technician for clinical specimens from which Syncephalastrum was isolated. A clinical isolate was sent to the Centers for Disease Control and Prevention (CDC) for fungal species identification by culture morphology.

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Results

Case Ascertainment

We identified the cases of eight patients whose ages ranged from 17 to 74 years old (Table 1). Five patients had symptoms compatible with an infectious process: bronchitis, pneumonia, sepsis, otitis externa, and sinusitis. Two patients had abnormal radiographic findings prompting a diagnostic bronchoscopy: 1) patient D had radiographic evidence of pulmonary consolidation by computed tomography (CT) scan and fever, and 2) patient E had images of a lung mass on plain chest radiograph and CT scan. One asymptomatic patient was identified as a result of a scheduled bronchoscopy and biopsy for follow-up of his lung transplant as part of a transplant protocol (patient C).

Since January 1, 2004, Syncephalastrum had not been reported in any clinical specimens before the hurricanes. Specimens from the eight patients were obtained from September 12, 2005, to January 12, 2006, in both inpatient and outpatient locations (Table 2 and Fig. 1). Sources of the specimens included BALs, endotracheal aspirate, sputum, ear swab, and nasal swab. The BAL of patient B was negative for fungal elements. Histopathological evaluation of bronchoscopic biopsy specimens obtained from two patients (patients C and E) was negative for fungal elements, with no evidence of tissue invasion. Three patients had a subsequent clinical specimen (two BALs and 1 endotracheal aspirate) obtained within 3 days of the initial positive culture result; no Syncephalastrum was isolated from these subsequent clinical specimens.

All symptomatic patients were diagnosed as having non-mold infections (eg, bacteremia, Candida otitis) and recovered without treatment appropriate for zygomycetes. Although the two lung transplant patients (patients C and F) were on long-term antifungal prophylaxis with itraconazole (200 mg/d), both patients had subtherapeutic serum levels (<0.3 μg/mL) of itraconazole and hydroxyitraconazole in March 2006. Patients C, D, and E did not have symptoms compatible with an invasive mold infection. None of the patients received any antifungal treatment as a result of the positive Syncephalastrum cultures. Thus, all cases were categorized as colonized (ie, present in the patients) but not causing illness or infection.

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Evaluation of Exposure

We interviewed seven of eight patients (Table 1). Only patient D reported significant exposures to mold after the hurricanes. On the day of presentation, he had been remediating a moldy house without wearing a respirator. The other patients reported minimal or no exposures to mold. Patient E had briefly visited his flooded home once to recover some items prior to his visit to the OCF. Patient G was a contractor who had visited several damaged buildings prior to his visit to the OCF. The remaining four patients reported no exposures to moldy indoor environments prior to the date that their specimens were collected. We were unable to contact patient B, a homeless woman who had been wading chest high in floodwater immediately before being admitted to the emergency department of the OCF (as noted in her medical chart).

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Laboratory Investigation

All clinical specimens were processed and analyzed at the on-site OCF clinical microbiology laboratory. Clinical specimens were cultured on blood and MacConkey agar plates (for routine culture) incubated for 2 days at 30°C or Sabouraud dextrose and mycobiotic agar plates (for fungal culture) incubated for 30 days at 30°C. CDC confirmed that the clinical isolate from patient F was Syncephalastrum.

The number of ENT and respiratory clinical specimens submitted to the microbiology laboratory for routine or fungal culture ranged from 1 to 16 per day (Fig. 1). The frequency of recovery of Syncephalastrum ranged from 6% to 33% of the ENT and respiratory specimens submitted on the days that Syncephalastrum was isolated during the period of investigation. Syncephalastrum was not reported in any clinical specimens between January 1, 2004, and September 12, 2005. Immediately after the hurricane, there was a marked decrease in the number of specimens submitted. The numbers returned to pre-hurricane levels on September 12, 2006, when many of the clinicians were allowed to return to work. Other than two specimens from two patients (sputum and a BAL) that were submitted on September 12, 2005, at 2:06 pm and 2:08 pm, respectively, no other clustering of Syncephalastrum isolation by time was apparent (Fig. 1). These two specimens submitted on September 12, 2005, were prepared using different tools and techniques.

All of the specimens were obtained in different locations (both inpatient and outpatient facilities) at the OCF (Table 2). Five different types of specimens were submitted. Growth on fungal-specific media was not quantified. On the routine cultures where growth was quantified (n = 4), growth ranged from 1 colony to slight (ie, in the first swab quadrant of the culture plate).

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Discussion

Syncephalastrum, of the class Zygomycetes, is a hydrophilic and thermotolerant mold that is able to germinate and sporulate within days when grown on substrates of high water activity.13Syncephalastrum is considered to be of very low pathogenicity.10 Mice and rabbits experimentally exposed to Syncephalastrum spores intravenously did not develop invasive disease.14,15 In a study of porcine mycotic pneumonia, the researchers concluded that the 29 pathogenic species of fungi, including Syncephalastrum, that were isolated from the lungs without demonstration of tissue infiltration, settled there as commensals.16

Previous reports of Syncephalastrum infections in humans have most often been associated with poorly controlled diabetes or trauma and limited to cutaneous and corneal infections.4,5,7 Recently, a Syncephalastrum wound infection was reported in an immunocompetent man who was impaled with a steel rod.6 A previously reported intracavitary pulmonary fungal ball attributed to Syncephalastrum was subsequently properly identified as Aspergillus niger.17,18

We identified eight patients with a positive culture result for Syncephalastrum from a clinical specimen between September 12, 2005, and January 12, 2006. Specimen or laboratory contamination does not appear to have occurred with these specimens, given the variability in the type of specimen and specimen collection dates, methods, and locations. On the four routine cultures, growth only occurred in the first streaked quadrant of the culture plate, which is not consistent with laboratory contamination where airborne spores fall onto culture plates by chance, resulting in random growth patterns. In addition, several ENT and respiratory specimens were processed on the same days that did not isolate Syncephalastrum (Fig. 1).

The two lung transplant patients (patients C and F) were prescribed prophylactic itraconazole (200 mg/d) in addition to routine immunosuppressive drugs (eg, tacrolimus). Zygomycetes are classically considered not susceptible to older azole drugs; the data are limited for Syncephalastrum.10 Some studies have shown Syncephalastrum to be susceptible to many antifungal agents in vitro, including itraconazole.9,19,20 In a study of lung transplant patients, prophylactic itraconazole (200 mg/dose twice daily) significantly reduced the number of positive BAL cultures for fungi (ie, Aspergillus and Candida) but did not affect the rate of infection in the patients.21 The role of itraconazole in preventing invasive disease in these two lung transplant patients is not clear but appears to be negligible given the dosage and the undetectable serum levels.

It is reasonable to presume that exposures to the extensive mold contamination after Hurricanes Katrina and Rita could cause a variety of adverse health outcomes, both infectious and allergic. Findings from our investigation suggest that the cases of Syncephalastrum reported here represent transient colonization in an immunocompetent person with heavy exposure to mold as well as in immunocompromised individuals with minimal or no mold exposures. Syncephalastrum appears to be of low pathogenicity; however, it is capable of colonizing returning NOLA residents. Detection of Syncephalastrum in clinical samples was not an indication of invasive disease. Specific testing for this mold in clinical samples is unwarranted, even under these extraordinary conditions of exposure in New Orleans.

The health outcomes of heavy exposures to traditionally more pathogenic molds, however, are still uncertain for post-hurricane NOLA residents. Molds that are more pathogenic than Syncephalastrum, such as Aspergillus fumigatus and Aspergillus niger, have also been reported in the air of NOLA flood-damaged homes after the hurricanes.12 Hospitals in the greater New Orleans area should continue to be vigilant in identifying invasive mold infections as NOLA residents return to moldy homes and buildings. Until more evidence becomes available regarding the risk of disease from various intensities of exposures to pathogenic molds, individuals with underlying respiratory diseases or with weakened immune systems (either from treatment with immunosuppressive drugs or from diseases), should follow recommended guidelines when entering moldy buildings, such as avoiding exposures completely, using protective equipment (eg, respirators and gloves), or limiting time spent in moldy environments.2

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Acknowledgments

The authors are indebted to Dr David Warnock for his insight; Dr Snigdha Vallabhaneni for her assistance with data collection; and Ms Janine Chapman, Ms Jane Flanagan, Ms Wanda Eppling, and Mr Michael King for their technical assistance during the investigation. The authors are also indebted to the patients who agreed to be interviewed about their exposures to mold. The work presented here was done as part of routine public health investigations conducted by the CDC and infection control investigations conducted by the OCF.

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