Mixed Pulmonary Infection with Strongyloides stercoralis and Blastomyc
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《微生物临床杂志》
Pathology and Laboratory Medicine, Department of Veterans Affairs Medical Center, Louisville, Kentucky
Division of Infectious Diseases, Department of Medicine, University of Louisville School of Medicine, Louisville, Kentucky
ABSTRACT
We report the first case of mixed pulmonary infection with Strongyloides stercoralis and Blastomyces dermatitidis. Histopathology from the lung biopsy showed structures consistent with B. dermatitidis and S. stercoralis. A parasitology exam from a bronchi alveolar lavage yielded an immature rhabditiform larva and female worm. Fungal cultures grew B. dermatitidis.
CASE REPORT
The patient is a 55-year-old male rural hermit, who had worked in several outdoor jobs with no permanent residence. The patient first visited the veterans hospital in Hawaii and presented with depression and a history of a persistent 5-week cough. His chest X-ray demonstrated a right upper lobe mass, which was interpreted and treated on an outpatient basis as community-acquired pneumonia. The patient presented to the Louisville, Kentucky, Veterans Affairs Medical Center for follow-up care due to worsening of his respiratory condition. He was admitted for evaluation of night cough and occasional vomiting over a 5-week period. His physical examination was normal. Computed tomography of the chest showed a large, soft, tissue mass opacity in the left upper lobe of the lung and several slightly enlarged hilar and mediastinal lymph nodes. A chest X-ray showed a 5- to 6-cm mass in the left upper lobe and no residual finding in the right lobe. Laboratory findings demonstrated a white blood cell count of 12.8 x 109/liter (neutrophils, 9.3 x 109/liter; monocytes, 1.0 x 109/liter; lymphocytes, 2.3 x 109/liter; eosinophils, 0.1 x 109/liter; and basophils, 0.1 x 109/liter). Blood cultures and bronchoalveolar lavage (BAL) cultures were negative for bacterial pathogens. BAL fungal cultures were obtained but remained negative for 5 weeks. No stool specimens were submitted for parasitology exam. The initial parasitological exam of the BAL was negative for ova and parasites. A transbronchial biopsy of the lung lesion yielded four, brown to white-tan, irregular tissue fragments, ranging from 0.1 to 0.2 cm and aggregately measuring 0.6 by 0.4 by 0.3 cm. The entirety was embedded in paraffin, thin-sectioned, and stained with hematoxylin-eosin, periodic acid-Schiff (PAS), Grocott-methenamine-silver (GMS), and acid-fast stain. Papanicolaou-stained concentrated smears (Thinprep) and cell blocks were prepared from the BAL; sections from cell blocks were stained similar to the biopsy sections.
Microscopic examination of the biopsy sections revealed most of the pulmonary parenchyma to be replaced by nonnecrotizing giant-cell granulomata, acute and chronic inflammatory infiltrate, and fibrosis. Some giant cells showed spherical to ovoid structures with thick outer membrane/capsules and one to few, small internal (nuclear) particles. These structures (8 to 15 μm in diameter) were negative with acid-fast stain but showed variable or weakly positive reactions with PAS and GMS stains; their features were suggestive of the dimorphic fungus Blastomyces dermatitidis (Fig. 1A and B) (1). Further examination revealed that some of these yeast-like structures were more consistent with the morphology of cross-sectioned Strongyloides (Fig. 1A and C). Some demonstrated a cuticle-like membrane with variable to no internal morphology, surrounded by an outer capsular material. Other structures showed extensive internal morphology with a rigid membrane that sheared during the histological sectioning (Fig. 1A, lower left star). With this presentation, the BAL fluid was reexamined for the presence of parasites. Three milliliters of the BAL fluid was concentrated to 0.5 ml by centrifugation and examined by iodine wet mount. One immature rhabditiform larva and female worm (Fig. 2) were observed. We obtained additional consultation from the Armed Forces Institute of Pathology, Bethesda, MD, and sent representative material, including photomicrographs. Their staff concurred with our observations that some structures seen were consistent with B. dermatitidis and that others were consistent with parasite larvae.
Fungal cultures yielded B. dermatitidis at 5 weeks. Cultures of B. dermatitidis on brain heart infusion blood agar failed to convert at 37°C to the yeast phase. The isolate identity was confirmed as B. dermatitidis using AccuProbe genetic hybridization analysis (Gen-Probe, Inc., San Diego, CA).
The patient was initially placed on a course of ivermectin for Strongyloides infection while awaiting confirmation of fungal culture results. The patient was scheduled to return to the clinic in 2 weeks but did not return and was not located.
In this report, we have shown evidence of a mixed pulmonary infection with Strongyloides stercoralis and B. dermatitidis. Our observations presented an unusual morphology for S. stercoralis. The female worm and rhabditiform larva both appeared as immature stages. We propose that the unusual influences of nourishment and temperature within a granulomatous lung may have caused changes in the life cycle and morphology of this organism. Gardner et al. reported that aging of Strongyloides ratti females resulted in unusual morphological forms affected by temperature (3). Likewise, Shiwaku et al. reported that rhabditiform larvae of S. stercoralis developed predominantly to free-living females at incubation temperatures of 15 to 30°C and low fecal dilutions, but filariform larvae appeared mainly under extreme conditions such as high temperatures (10). The host immune response was shown to affect the developmental stages of S. ratti, causing a reduction in parasite size as well as reproductive relocation within the gut (11). Strongyloides often occurs in mixed infections. The most common mixed infections with Strongyloides occur with gram-negative bacteria as they are carried by the migrating larvae from the intestine to the blood and lungs (7, 8). Other investigators have noted that pleural space infections may be complicated by mixed infections with rare organisms (2).
The difficulty of establishing a diagnosis by histopathologic evaluation can lead to erroneous results complicated by "pseudomicrobes" (4). Images observed in histopathology and cytopathology can mimic mycotic agents, parasites, bacteria, or viruses (5). As demonstrated here, open communications between the pathologist and microbiologist allowed recovery of both pathogens. A physician's direct communications with the laboratory are essential to ensure the best patient care (9). They often prompt the laboratory to examine the specimen with techniques that are more specialized for the recovery of specific microorganisms. Failure to explore all microbiological methods for the recovery of nematodes can result in death (6).
We believe this report to be unique and important because it describes the first case of pulmonary infection with both S. stercoralis and B. dermatitidis. It is interesting because of the recovery from the BAL fluid of the fungus and parasite with corroborating histopathology. This report adds to our knowledge of parasitic infections and their clinical diagnosis mediated by concerted efforts of physicians and laboratory specialists.
ACKNOWLEDGMENTS
This work was performed at the Department of Veterans Affairs Medical Center, Louisville, KY. We acknowledge James E. Lay for his technical assistance in the recovery of both isolates.
FOOTNOTES
Corresponding author. Mailing address: Pathology and Laboratory Medicine, Department of Veterans Affairs Medical Center, 800 Zorn Ave., Louisville, KY 40206.
Published ahead of print on 6 September 2006.
REFERENCES
Chapman, S. W. 2000. Blastomyces dermatitidis, p. 2733-2746. In G. L. Mandell, J. E. Bennett, and R. Dolin (ed.), Principles and practice of infectious diseases, 5th ed. Churchill Livingstone, Philadelphia, Pa.
Everts, R. J., and L. B. Reller. 1999. Pleural space infections: microbiology and antimicrobial therapy. Semin. Respir. Infect. 14:18-30.
Gardner, M. P., D. Gems, and M. E. Viney. 2004. Aging in a very short-lived nematode. Exp. Gerontol. 39:1267-1276.
Gorelkin, L., and F. W. Chandler. 1988. Pseudomicrobes: some potential diagnostic pitfalls in the histopathologic assessment of inflammatory lesions. Hum. Pathol. 19:954-959.
Hofman, P., and M. Huerre. 2001. Diagnostic pitfalls in infectious disease pathology. Ann. Pathol. 21:411-424.
Lemos, L. B., Z. Qu, R. Laucirica, and H. L. Fred. 2003. Hyper infection syndrome in strongyloidiasis: report of two cases. Ann. Diagn. Pathol. 7:87-94.
Mahmoud, A. A. F. 2000. Intestinal nematodes (roundworms), p. 2938-2943. In G. L. Mandell, J. E. Bennett, and R. Dolin (ed.), Principles and practice of infectious diseases, 5th ed. Churchill Livingstone, Philadelphia, Pa.
Pornsuriyasak, P., K. Niticharoenpong, and A. Sakapibunnan. 2004. Disseminated strongyloidiasis successfully treated with extended duration ivermectin combined with albendazole: a case report of intractable strongyloidiasis. Southeast Asian J. Trop. Med. Public Health 35:531-534.
Saubolle, M. A., and P. P. McKellar. 2001. Laboratory diagnosis of community-acquired lower respiratory tract infection. Infect. Dis. Clin. North. Am. 15:1025-1045.
Shiwaku, K., Y. Chigusa, T. Kadosaka, and K. Kaneko. 1988. Factors influencing development of free-living generations of Strongyloides stercoralis. Parasitology 97:129-138.
Wilkes, C. P., F. J. Thompson, M. P. Gardner, S. Paterson, and M. E. Viney. 2004. The effect of the host immune response on the parasitic nematode Strongyloides ratti. Parasitology 128:661-669.(Carmen Sciortino, Rawhi Omar, and Rafael)
Division of Infectious Diseases, Department of Medicine, University of Louisville School of Medicine, Louisville, Kentucky
ABSTRACT
We report the first case of mixed pulmonary infection with Strongyloides stercoralis and Blastomyces dermatitidis. Histopathology from the lung biopsy showed structures consistent with B. dermatitidis and S. stercoralis. A parasitology exam from a bronchi alveolar lavage yielded an immature rhabditiform larva and female worm. Fungal cultures grew B. dermatitidis.
CASE REPORT
The patient is a 55-year-old male rural hermit, who had worked in several outdoor jobs with no permanent residence. The patient first visited the veterans hospital in Hawaii and presented with depression and a history of a persistent 5-week cough. His chest X-ray demonstrated a right upper lobe mass, which was interpreted and treated on an outpatient basis as community-acquired pneumonia. The patient presented to the Louisville, Kentucky, Veterans Affairs Medical Center for follow-up care due to worsening of his respiratory condition. He was admitted for evaluation of night cough and occasional vomiting over a 5-week period. His physical examination was normal. Computed tomography of the chest showed a large, soft, tissue mass opacity in the left upper lobe of the lung and several slightly enlarged hilar and mediastinal lymph nodes. A chest X-ray showed a 5- to 6-cm mass in the left upper lobe and no residual finding in the right lobe. Laboratory findings demonstrated a white blood cell count of 12.8 x 109/liter (neutrophils, 9.3 x 109/liter; monocytes, 1.0 x 109/liter; lymphocytes, 2.3 x 109/liter; eosinophils, 0.1 x 109/liter; and basophils, 0.1 x 109/liter). Blood cultures and bronchoalveolar lavage (BAL) cultures were negative for bacterial pathogens. BAL fungal cultures were obtained but remained negative for 5 weeks. No stool specimens were submitted for parasitology exam. The initial parasitological exam of the BAL was negative for ova and parasites. A transbronchial biopsy of the lung lesion yielded four, brown to white-tan, irregular tissue fragments, ranging from 0.1 to 0.2 cm and aggregately measuring 0.6 by 0.4 by 0.3 cm. The entirety was embedded in paraffin, thin-sectioned, and stained with hematoxylin-eosin, periodic acid-Schiff (PAS), Grocott-methenamine-silver (GMS), and acid-fast stain. Papanicolaou-stained concentrated smears (Thinprep) and cell blocks were prepared from the BAL; sections from cell blocks were stained similar to the biopsy sections.
Microscopic examination of the biopsy sections revealed most of the pulmonary parenchyma to be replaced by nonnecrotizing giant-cell granulomata, acute and chronic inflammatory infiltrate, and fibrosis. Some giant cells showed spherical to ovoid structures with thick outer membrane/capsules and one to few, small internal (nuclear) particles. These structures (8 to 15 μm in diameter) were negative with acid-fast stain but showed variable or weakly positive reactions with PAS and GMS stains; their features were suggestive of the dimorphic fungus Blastomyces dermatitidis (Fig. 1A and B) (1). Further examination revealed that some of these yeast-like structures were more consistent with the morphology of cross-sectioned Strongyloides (Fig. 1A and C). Some demonstrated a cuticle-like membrane with variable to no internal morphology, surrounded by an outer capsular material. Other structures showed extensive internal morphology with a rigid membrane that sheared during the histological sectioning (Fig. 1A, lower left star). With this presentation, the BAL fluid was reexamined for the presence of parasites. Three milliliters of the BAL fluid was concentrated to 0.5 ml by centrifugation and examined by iodine wet mount. One immature rhabditiform larva and female worm (Fig. 2) were observed. We obtained additional consultation from the Armed Forces Institute of Pathology, Bethesda, MD, and sent representative material, including photomicrographs. Their staff concurred with our observations that some structures seen were consistent with B. dermatitidis and that others were consistent with parasite larvae.
Fungal cultures yielded B. dermatitidis at 5 weeks. Cultures of B. dermatitidis on brain heart infusion blood agar failed to convert at 37°C to the yeast phase. The isolate identity was confirmed as B. dermatitidis using AccuProbe genetic hybridization analysis (Gen-Probe, Inc., San Diego, CA).
The patient was initially placed on a course of ivermectin for Strongyloides infection while awaiting confirmation of fungal culture results. The patient was scheduled to return to the clinic in 2 weeks but did not return and was not located.
In this report, we have shown evidence of a mixed pulmonary infection with Strongyloides stercoralis and B. dermatitidis. Our observations presented an unusual morphology for S. stercoralis. The female worm and rhabditiform larva both appeared as immature stages. We propose that the unusual influences of nourishment and temperature within a granulomatous lung may have caused changes in the life cycle and morphology of this organism. Gardner et al. reported that aging of Strongyloides ratti females resulted in unusual morphological forms affected by temperature (3). Likewise, Shiwaku et al. reported that rhabditiform larvae of S. stercoralis developed predominantly to free-living females at incubation temperatures of 15 to 30°C and low fecal dilutions, but filariform larvae appeared mainly under extreme conditions such as high temperatures (10). The host immune response was shown to affect the developmental stages of S. ratti, causing a reduction in parasite size as well as reproductive relocation within the gut (11). Strongyloides often occurs in mixed infections. The most common mixed infections with Strongyloides occur with gram-negative bacteria as they are carried by the migrating larvae from the intestine to the blood and lungs (7, 8). Other investigators have noted that pleural space infections may be complicated by mixed infections with rare organisms (2).
The difficulty of establishing a diagnosis by histopathologic evaluation can lead to erroneous results complicated by "pseudomicrobes" (4). Images observed in histopathology and cytopathology can mimic mycotic agents, parasites, bacteria, or viruses (5). As demonstrated here, open communications between the pathologist and microbiologist allowed recovery of both pathogens. A physician's direct communications with the laboratory are essential to ensure the best patient care (9). They often prompt the laboratory to examine the specimen with techniques that are more specialized for the recovery of specific microorganisms. Failure to explore all microbiological methods for the recovery of nematodes can result in death (6).
We believe this report to be unique and important because it describes the first case of pulmonary infection with both S. stercoralis and B. dermatitidis. It is interesting because of the recovery from the BAL fluid of the fungus and parasite with corroborating histopathology. This report adds to our knowledge of parasitic infections and their clinical diagnosis mediated by concerted efforts of physicians and laboratory specialists.
ACKNOWLEDGMENTS
This work was performed at the Department of Veterans Affairs Medical Center, Louisville, KY. We acknowledge James E. Lay for his technical assistance in the recovery of both isolates.
FOOTNOTES
Corresponding author. Mailing address: Pathology and Laboratory Medicine, Department of Veterans Affairs Medical Center, 800 Zorn Ave., Louisville, KY 40206.
Published ahead of print on 6 September 2006.
REFERENCES
Chapman, S. W. 2000. Blastomyces dermatitidis, p. 2733-2746. In G. L. Mandell, J. E. Bennett, and R. Dolin (ed.), Principles and practice of infectious diseases, 5th ed. Churchill Livingstone, Philadelphia, Pa.
Everts, R. J., and L. B. Reller. 1999. Pleural space infections: microbiology and antimicrobial therapy. Semin. Respir. Infect. 14:18-30.
Gardner, M. P., D. Gems, and M. E. Viney. 2004. Aging in a very short-lived nematode. Exp. Gerontol. 39:1267-1276.
Gorelkin, L., and F. W. Chandler. 1988. Pseudomicrobes: some potential diagnostic pitfalls in the histopathologic assessment of inflammatory lesions. Hum. Pathol. 19:954-959.
Hofman, P., and M. Huerre. 2001. Diagnostic pitfalls in infectious disease pathology. Ann. Pathol. 21:411-424.
Lemos, L. B., Z. Qu, R. Laucirica, and H. L. Fred. 2003. Hyper infection syndrome in strongyloidiasis: report of two cases. Ann. Diagn. Pathol. 7:87-94.
Mahmoud, A. A. F. 2000. Intestinal nematodes (roundworms), p. 2938-2943. In G. L. Mandell, J. E. Bennett, and R. Dolin (ed.), Principles and practice of infectious diseases, 5th ed. Churchill Livingstone, Philadelphia, Pa.
Pornsuriyasak, P., K. Niticharoenpong, and A. Sakapibunnan. 2004. Disseminated strongyloidiasis successfully treated with extended duration ivermectin combined with albendazole: a case report of intractable strongyloidiasis. Southeast Asian J. Trop. Med. Public Health 35:531-534.
Saubolle, M. A., and P. P. McKellar. 2001. Laboratory diagnosis of community-acquired lower respiratory tract infection. Infect. Dis. Clin. North. Am. 15:1025-1045.
Shiwaku, K., Y. Chigusa, T. Kadosaka, and K. Kaneko. 1988. Factors influencing development of free-living generations of Strongyloides stercoralis. Parasitology 97:129-138.
Wilkes, C. P., F. J. Thompson, M. P. Gardner, S. Paterson, and M. E. Viney. 2004. The effect of the host immune response on the parasitic nematode Strongyloides ratti. Parasitology 128:661-669.(Carmen Sciortino, Rawhi Omar, and Rafael)