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Severe cutaneous aspergillosis in a premature neonate linked to nonsterile disposable glove contamination?
American Journal of Infection Control 40 (2012) 465-7
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Severe cutaneous aspergillosis in a premature neonate linked to nonsterile disposable glove contamination? Claire Stock MD a, Magali Veyrier MD a, Hélène Raberin MD b, Pascal Fascia MD c, Isabelle Rayet MD a, Marie Pierre Lavocat MD a, Georges Teyssier MD, PhD a, Philippe Berthelot MD, MPH, PhD c, * a b c
Neonatal Intensive Care Unit, University Hospital of Saint-Etienne, Saint-Etienne, France Mycology Laboratory, University Hospital of Saint-Etienne, Saint-Etienne, France Department of Infectious Diseases, Infection Control Unit, University Hospital of Saint-Etienne, Saint-Etienne, France
Key Words: Aspergillus fumigatus Intensive care Newborn Invasive aspergillosis Intensive care unit
After having eliminated a dysfunction of the hospital’s ventilation system and any other possible environmental reservoir, the investigation of a fatal case of primary cutaneous aspergillosis in a neonate with extremely low birth weight led to the conclusion that nonsterile disposable gloves kept stored in their native packages were the likely source of contamination. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Infection with Aspergillus spp can cause primary cutaneous aspergillosis in neonates of extremely low birth weight (ELBW) because of these neonates’ decreased qualitative immune defenses and defects in the skin barrier. The presence of building work near hospital wards receiving immunocompromised patients is one of the main risk factors for developing invasive aspergillosis (IA). We report the investigation of a fatal case of primary cutaneous aspergillosis complicated with IA in an ELBW neonate. CASE REPORT Six days after delivery at 24 weeks’ gestation, an ELBW neonate (birth weight, 600 g) developed necrotic skin lesions. These lesions invaded the back, perineum, and axillae and were complicated by the occurrence of pneumonia. A fumigatus was isolated in skin lesions and bronchoalveolar lavage fluid. Despite the initiation of intravenous antifungal therapy, the neonate died due to multiorgan failure. Necropsy confirmed a diagnosis of primary cutaneous aspergillosis complicated with IA.1 Setting The neonatal intensive care unit (NICU) of the University Hospital of Saint-Etienne contains 3 main areas occupied by 4 incubators, for * Address correspondence to Philippe Berthelot, MD, MPH, PhD, Department of Infectious Diseases, Infection Control Unit and Laboratory of Microbiology, 42055 CHU Saint Etienne Cedex 02, France. E-mail address: [email protected] (P. Berthelot). Conflict of interest: None to report.
a total of 12 beds (Fig 1). The ventilation system includes highefficiency particulate air filters. Moreover, the unit is equipped with an anteroom to maintain the air pressure at a higher level than the hallway outside the unit. All windows are sealed against air leaks. As a rule, health care workers use an alcoholic handrub for hand hygiene, and the introduction of cardboard boxes in the unit is strictly forbidden. Moreover, environmental surveillance is performed monthly, including analysis of at least 12 mycologic samples obtained by swabbing 10-cm2 surface areas in the patients’ close environment, on air vents, and on metallic surfaces known to retain contamination by spores. Water samples from the unit are checked for the presence of pathogens every 3 months. Because of outside renovation work, precautions aimed at preventing dust infiltration into the unit had been reinforced before the start of this study. Mycologic analysis Samples were cultured on Sabouraud dextrose agar plates containing chloramphenicol (Sabouraud chloramphenicol, SAB CHL2-F; bioMérieux, Craponne, France). The plates were incubated at 37 C for 1 day to promote the growth of A fumigatus, and then incubated at 25 C for another 4 days. Colonies were identified at the genus level for filamentous fungi and at the species level for Aspergillus spp. Investigation After the occurrence of the present case, an investigation was conducted that included a review of medical and microbiological
0196-6553/$36.00 - Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2011.05.013
466
C. Stock et al. / American Journal of Infection Control 40 (2012) 465-7
Fig 1. Positive results (expressed as CFU/10 cm2 of surface area) of mycologic cultures obtained in the NICU. More than 140 surface samplings were performed. Sterile hyphae and Aspergillus spp contamination of surfaces are represented by cross-hatched and gray symbols, respectively.
files and an exhaustive check of the NICU ventilation system and of the plastic barriers protecting the NICU from the area of renovation work. Additional environmental samples were obtained in various locations, including the labor and delivery area, incubator used for transfer of the neonate, incubator and areas near the infant, surfaces in the unit where care was provided, nonsterile care devices (eg, diapers, disposable strips, creams, compresses), and disposable towels used for hand drying. Because we had already reported bacterial and fungal contamination of disposable nonsterile gloves stored in unopened boxes,2 we also targeted these, obtaining samples from the surfaces of new boxes stored in the clean supply room of the NICU and from gloves located at the top and in the middle of these boxes. All of the mycologic cultures were performed in a class II microbiological safety cabinet to exclude airborne contamination.
particularly in the peripheral hallway surrounding the unit, only a few surface samples from inside the NICU were found to be positive (with low cell counts). Colonies of A fumigatus also were recovered from the top glove of an unopened box of nonpowdered latex nonsterile disposable gloves. Out of 3 other tested boxes of gloves from 3 separate batches, 2 yielded gloves contaminated by A versicolor or A niger (Table 1). Sampling of the surfaces of the clean supply room and of unopened glove boxes revealed no A fumigatus contamination. In accordance with NICU practice, it was decided to use only sterile gloves when delivering care to neonates weighing <1,000 g or born at <28 weeks’ gestation until 15 days of life, at which point the skin provides a sufficient barrier. During the 24 months following implementation of this measure, no A fumigatus contamination of NICU surfaces was observed, and no other cases of aspergillosis were recorded.
RESULTS No dysfunction of the NICU ventilation system was detected. More than 140 environmental samples were tested. No A fumigatus contamination was documented, with the exception of the area where the neonate was located (Fig 1); after cleaning of this area, no additional strains of Aspergillus spp were recovered. Although high sterile hyphae contamination was observed outside the NICU,
DISCUSSION AND CONCLUSION Despite the global increase of fungal infections, primary cutaneous aspergillosis is a rare event in the NICU.3-6 Most of the reported cases occurred in ELBW neonates and were hospitalacquired. Renovation work is a common source of environmental
C. Stock et al. / American Journal of Infection Control 40 (2012) 465-7
467
Table 1 Fungal contamination of nonsterile disposable gloves from unopened boxes from 3 different batches stored in the NICU Aspergillus spp (CFU/80 mL) per glove Position of the glove in the box
Box 1 (batch 1)
Box 2 (batch 1)
Box 3 (batch 2)
Box 4 (batch 3)
Top Mid
A fumigatus (3) 0
0 0
0 A. niger (2)
A versicolor (1) A niger (1) A versicolor (1)
0 means that the search for fungi was negative.
contamination by Aspergillus spp,7 but preventive measures using plastic barriers and reinforced surveillance can decrease this risk.8 In the present study, we did not isolate Aspergillus spp in the NICU environment, with the exception of the neonate’s immediate surroundings. Because our samples were obtained within a few hours after the neonate’s death and because of negative results in samples obtained from the same locations 12 days earlier, we deemed the contamination of surfaces near the neonate to be secondary to the neonate’s extensive cutaneous aspergillosis. Thus, we hypothesized that the neonate’s skin could have been contaminated by nonsterile devices or material used while providing care. A disposable nonsterile glove from an unopened stored box was found to be contaminated with A fumigatus. Such a glove, used notably for diaper changes, could have contaminated the neonate’s skin. Because the skin barrier is very thin in EBLW neonates, skin contamination can lead to severe aspergillosis. Singer et al9 reported 4 cases of IA in premature neonates linked to the contamination of latex finger stalls. In a previous study,1 we investigated the microbiological contamination of disposable nonsterile gloves that had been stored in their native packages. A wide variety of spore-forming and nonespore-forming bacteria was recovered, including Bacillus cereus and Clostridium perfringens; A versicolor was recovered in 1 sample. We had concluded this previous study by recommending the use of sterile disposable gloves for care procedures involving mucosa in highly immunocompromised patients. The present case of fatal primary cutaneous aspergillosis in an ELBW neonate raises the question of whether the exclusive use of sterile gloves should be extended to this category of fragile patients, even when providing noninvasive care measures.
Acknowledgment We thank Bruno Pozzetto for his help in editing the manuscript.
References 1. Stock C, Veyrier M, Magnin-Verschelde S, Duband S, Lavocat MP, Teyssier G, et al. Primary cutaneous aspergillosis complicated with invasive aspergillosis in an extremely preterm infant: case report and literature review. Arch Pediatr 2010; 17:1455-9. 2. Berthelot P, Dietemann J, Fascia P, Ros A, Mallaval FO, Lucht F, et al. Bacterial contamination of nonsterile disposable gloves before use. Am J Infect Control 2006;34:128-30. 3. James MJ, Lasker BA, McNeil MM, Shelton M, Warnock DW, Reiss E. Use of a repetitive DNA probe to type clinical and environmental isolates of Aspergillus flavus from a cluster of cutaneous infections in a neonatal intensive care unit. J Clin Microbiol 2000;38:3612-8. 4. Papouli M, Roilides E, Bibashi E, Andreou A. Primary cutaneous aspergillosis in neonates: case report and review. Clin Infect Dis 1996;22:1102-4. 5. Groll AH, Jaeger G, Allendorf A, Herrman G, Schloesser R, von Loewenich V. Invasive pulmonary aspergillosis in a critically ill neonate: case report and review of invasive aspergillosis during the first 3 months of life. Clin Infect Dis 1998;27:437-52. 6. Woodruff CA, Hebert AA. Neonatal primary cutaneous aspergillosis: case report and review of the literature. Pediatr Dermatol 2002;19:439-44. 7. Mahieu LM, De Dooy JJ, Van Laer FA, Jansens H, Leven MM. A prospective study on factors influencing aspergillus spore load in the air during renovation works in a neonatal intensive care unit. J Hosp Infect 2000;45:191-7. 8. Berthelot P, Loulergue P, Raberin H, Turco M, Mounier C, Tran Manh Sung R, et al. Efficacy of environmental measures to decrease the risk of hospital-acquired aspergillosis in patients hospitalised in haematology wards. Clin Microbiol Infect 2006;12:738-44. 9. Singer S, Singer D, Ruchel R, Mergeryan H, Schmidt U, Harms K. Outbreak of systemic aspergillosis in a neonatal intensive care unit. Mycoses 1998;41:223-7.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Severe cutaneous aspergillosis in a premature neonate linked to nonsterile disposable glove contamination? Claire Stock MD a, Magali Veyrier MD a, Hélène Raberin MD b, Pascal Fascia MD c, Isabelle Rayet MD a, Marie Pierre Lavocat MD a, Georges Teyssier MD, PhD a, Philippe Berthelot MD, MPH, PhD c, * a b c
Neonatal Intensive Care Unit, University Hospital of Saint-Etienne, Saint-Etienne, France Mycology Laboratory, University Hospital of Saint-Etienne, Saint-Etienne, France Department of Infectious Diseases, Infection Control Unit, University Hospital of Saint-Etienne, Saint-Etienne, France
Key Words: Aspergillus fumigatus Intensive care Newborn Invasive aspergillosis Intensive care unit
After having eliminated a dysfunction of the hospital’s ventilation system and any other possible environmental reservoir, the investigation of a fatal case of primary cutaneous aspergillosis in a neonate with extremely low birth weight led to the conclusion that nonsterile disposable gloves kept stored in their native packages were the likely source of contamination. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Infection with Aspergillus spp can cause primary cutaneous aspergillosis in neonates of extremely low birth weight (ELBW) because of these neonates’ decreased qualitative immune defenses and defects in the skin barrier. The presence of building work near hospital wards receiving immunocompromised patients is one of the main risk factors for developing invasive aspergillosis (IA). We report the investigation of a fatal case of primary cutaneous aspergillosis complicated with IA in an ELBW neonate. CASE REPORT Six days after delivery at 24 weeks’ gestation, an ELBW neonate (birth weight, 600 g) developed necrotic skin lesions. These lesions invaded the back, perineum, and axillae and were complicated by the occurrence of pneumonia. A fumigatus was isolated in skin lesions and bronchoalveolar lavage fluid. Despite the initiation of intravenous antifungal therapy, the neonate died due to multiorgan failure. Necropsy confirmed a diagnosis of primary cutaneous aspergillosis complicated with IA.1 Setting The neonatal intensive care unit (NICU) of the University Hospital of Saint-Etienne contains 3 main areas occupied by 4 incubators, for * Address correspondence to Philippe Berthelot, MD, MPH, PhD, Department of Infectious Diseases, Infection Control Unit and Laboratory of Microbiology, 42055 CHU Saint Etienne Cedex 02, France. E-mail address: [email protected] (P. Berthelot). Conflict of interest: None to report.
a total of 12 beds (Fig 1). The ventilation system includes highefficiency particulate air filters. Moreover, the unit is equipped with an anteroom to maintain the air pressure at a higher level than the hallway outside the unit. All windows are sealed against air leaks. As a rule, health care workers use an alcoholic handrub for hand hygiene, and the introduction of cardboard boxes in the unit is strictly forbidden. Moreover, environmental surveillance is performed monthly, including analysis of at least 12 mycologic samples obtained by swabbing 10-cm2 surface areas in the patients’ close environment, on air vents, and on metallic surfaces known to retain contamination by spores. Water samples from the unit are checked for the presence of pathogens every 3 months. Because of outside renovation work, precautions aimed at preventing dust infiltration into the unit had been reinforced before the start of this study. Mycologic analysis Samples were cultured on Sabouraud dextrose agar plates containing chloramphenicol (Sabouraud chloramphenicol, SAB CHL2-F; bioMérieux, Craponne, France). The plates were incubated at 37 C for 1 day to promote the growth of A fumigatus, and then incubated at 25 C for another 4 days. Colonies were identified at the genus level for filamentous fungi and at the species level for Aspergillus spp. Investigation After the occurrence of the present case, an investigation was conducted that included a review of medical and microbiological
0196-6553/$36.00 - Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2011.05.013
466
C. Stock et al. / American Journal of Infection Control 40 (2012) 465-7
Fig 1. Positive results (expressed as CFU/10 cm2 of surface area) of mycologic cultures obtained in the NICU. More than 140 surface samplings were performed. Sterile hyphae and Aspergillus spp contamination of surfaces are represented by cross-hatched and gray symbols, respectively.
files and an exhaustive check of the NICU ventilation system and of the plastic barriers protecting the NICU from the area of renovation work. Additional environmental samples were obtained in various locations, including the labor and delivery area, incubator used for transfer of the neonate, incubator and areas near the infant, surfaces in the unit where care was provided, nonsterile care devices (eg, diapers, disposable strips, creams, compresses), and disposable towels used for hand drying. Because we had already reported bacterial and fungal contamination of disposable nonsterile gloves stored in unopened boxes,2 we also targeted these, obtaining samples from the surfaces of new boxes stored in the clean supply room of the NICU and from gloves located at the top and in the middle of these boxes. All of the mycologic cultures were performed in a class II microbiological safety cabinet to exclude airborne contamination.
particularly in the peripheral hallway surrounding the unit, only a few surface samples from inside the NICU were found to be positive (with low cell counts). Colonies of A fumigatus also were recovered from the top glove of an unopened box of nonpowdered latex nonsterile disposable gloves. Out of 3 other tested boxes of gloves from 3 separate batches, 2 yielded gloves contaminated by A versicolor or A niger (Table 1). Sampling of the surfaces of the clean supply room and of unopened glove boxes revealed no A fumigatus contamination. In accordance with NICU practice, it was decided to use only sterile gloves when delivering care to neonates weighing <1,000 g or born at <28 weeks’ gestation until 15 days of life, at which point the skin provides a sufficient barrier. During the 24 months following implementation of this measure, no A fumigatus contamination of NICU surfaces was observed, and no other cases of aspergillosis were recorded.
RESULTS No dysfunction of the NICU ventilation system was detected. More than 140 environmental samples were tested. No A fumigatus contamination was documented, with the exception of the area where the neonate was located (Fig 1); after cleaning of this area, no additional strains of Aspergillus spp were recovered. Although high sterile hyphae contamination was observed outside the NICU,
DISCUSSION AND CONCLUSION Despite the global increase of fungal infections, primary cutaneous aspergillosis is a rare event in the NICU.3-6 Most of the reported cases occurred in ELBW neonates and were hospitalacquired. Renovation work is a common source of environmental
C. Stock et al. / American Journal of Infection Control 40 (2012) 465-7
467
Table 1 Fungal contamination of nonsterile disposable gloves from unopened boxes from 3 different batches stored in the NICU Aspergillus spp (CFU/80 mL) per glove Position of the glove in the box
Box 1 (batch 1)
Box 2 (batch 1)
Box 3 (batch 2)
Box 4 (batch 3)
Top Mid
A fumigatus (3) 0
0 0
0 A. niger (2)
A versicolor (1) A niger (1) A versicolor (1)
0 means that the search for fungi was negative.
contamination by Aspergillus spp,7 but preventive measures using plastic barriers and reinforced surveillance can decrease this risk.8 In the present study, we did not isolate Aspergillus spp in the NICU environment, with the exception of the neonate’s immediate surroundings. Because our samples were obtained within a few hours after the neonate’s death and because of negative results in samples obtained from the same locations 12 days earlier, we deemed the contamination of surfaces near the neonate to be secondary to the neonate’s extensive cutaneous aspergillosis. Thus, we hypothesized that the neonate’s skin could have been contaminated by nonsterile devices or material used while providing care. A disposable nonsterile glove from an unopened stored box was found to be contaminated with A fumigatus. Such a glove, used notably for diaper changes, could have contaminated the neonate’s skin. Because the skin barrier is very thin in EBLW neonates, skin contamination can lead to severe aspergillosis. Singer et al9 reported 4 cases of IA in premature neonates linked to the contamination of latex finger stalls. In a previous study,1 we investigated the microbiological contamination of disposable nonsterile gloves that had been stored in their native packages. A wide variety of spore-forming and nonespore-forming bacteria was recovered, including Bacillus cereus and Clostridium perfringens; A versicolor was recovered in 1 sample. We had concluded this previous study by recommending the use of sterile disposable gloves for care procedures involving mucosa in highly immunocompromised patients. The present case of fatal primary cutaneous aspergillosis in an ELBW neonate raises the question of whether the exclusive use of sterile gloves should be extended to this category of fragile patients, even when providing noninvasive care measures.
Acknowledgment We thank Bruno Pozzetto for his help in editing the manuscript.
References 1. Stock C, Veyrier M, Magnin-Verschelde S, Duband S, Lavocat MP, Teyssier G, et al. Primary cutaneous aspergillosis complicated with invasive aspergillosis in an extremely preterm infant: case report and literature review. Arch Pediatr 2010; 17:1455-9. 2. Berthelot P, Dietemann J, Fascia P, Ros A, Mallaval FO, Lucht F, et al. Bacterial contamination of nonsterile disposable gloves before use. Am J Infect Control 2006;34:128-30. 3. James MJ, Lasker BA, McNeil MM, Shelton M, Warnock DW, Reiss E. Use of a repetitive DNA probe to type clinical and environmental isolates of Aspergillus flavus from a cluster of cutaneous infections in a neonatal intensive care unit. J Clin Microbiol 2000;38:3612-8. 4. Papouli M, Roilides E, Bibashi E, Andreou A. Primary cutaneous aspergillosis in neonates: case report and review. Clin Infect Dis 1996;22:1102-4. 5. Groll AH, Jaeger G, Allendorf A, Herrman G, Schloesser R, von Loewenich V. Invasive pulmonary aspergillosis in a critically ill neonate: case report and review of invasive aspergillosis during the first 3 months of life. Clin Infect Dis 1998;27:437-52. 6. Woodruff CA, Hebert AA. Neonatal primary cutaneous aspergillosis: case report and review of the literature. Pediatr Dermatol 2002;19:439-44. 7. Mahieu LM, De Dooy JJ, Van Laer FA, Jansens H, Leven MM. A prospective study on factors influencing aspergillus spore load in the air during renovation works in a neonatal intensive care unit. J Hosp Infect 2000;45:191-7. 8. Berthelot P, Loulergue P, Raberin H, Turco M, Mounier C, Tran Manh Sung R, et al. Efficacy of environmental measures to decrease the risk of hospital-acquired aspergillosis in patients hospitalised in haematology wards. Clin Microbiol Infect 2006;12:738-44. 9. Singer S, Singer D, Ruchel R, Mergeryan H, Schmidt U, Harms K. Outbreak of systemic aspergillosis in a neonatal intensive care unit. Mycoses 1998;41:223-7.