Journal of Tropical Medicine

Journal of Tropical Medicine / 2009 / Article

Case Report | Open Access

Volume 2009 |Article ID 969070 |

Gillian L. Genrich, Julu Bhatnagar, Christopher D. Paddock, Sherif R. Zaki, "Fatal Plasmodium falciparum, Clostridium perfringens, and Candida spp. Coinfections in a Traveler to Haiti", Journal of Tropical Medicine, vol. 2009, Article ID 969070, 6 pages, 2009.

Fatal Plasmodium falciparum, Clostridium perfringens, and Candida spp. Coinfections in a Traveler to Haiti

Academic Editor: Hans-Peter Beck
Received08 Oct 2008
Revised30 Jan 2009
Accepted17 Mar 2009
Published05 May 2009


Malaria is one of the most common causes of febrile illness in travelers. Coinfections with bacterial, viral, and fungal pathogens may not be suspected unless a patient fails to respond to malaria treatment. Using novel immunohistochemical and molecular techniques, Plasmodium falciparum, Clostridium perfringens, and Candida spp. coinfections were confirmed in a German traveler to Haiti. Plasmodium falciparum-induced ischemia may have increased this patient's susceptibility to C. perfringens and disseminated candidiasis leading to his death. When a patient presents with P. falciparum and shock and is unresponsive to malaria treatment, secondary infections should be suspected to initiate appropriate treatment.

1. Introduction

Plasmodium falciparum, an intraerythrocytic parasite that causes the most severe form of human malaria, is endemic to Haiti where it caused 32 739 infections and contributed to an estimated 741 malaria deaths in 2006 [13]. Malaria infection poses a risk to the 140 000 travelers from nonendemic countries that visit Haiti each year [4]. Progression to severe illness from initial symptoms of fever, headache, chills, and myalgia occurs rapidly through the phenomenon of sequestration, in which P. falciparum-infected erythrocytes attach to blood vessels and impede normal blood flow, particularly in the brain [5]. Poor perfusion leads to tissue ischemia, which may subsequently increase a patient’s susceptibility to secondary infections [5, 6] such as C. perfringens, and Candida spp. C. perfrignens is an anaerobic spore-forming bacillus that produces a virulent hemolytic alpha toxin [7] and causes gas gangrene, a potentially deadly infection characterized by fever, pain, edema, myonecrosis, and gas production [8]. And in a setting of tissue ischemia and necrosis, endogenous gut microflora such as Candida may translocate across the epithelial border and gain access to systemic circulation resulting in disseminated candidiasis [9].

Malaria coinfections with Leptospira spp., Coxiella burnetti, Brucella melitensis, and Streptococcus pneumoniae as well as with enteric bacteria (Eschericha coli and Salmonella, and Acinetobacter baumannii) have previously been reported [1014]. To our knowledge, this report describes the first fatal coinfection of P. falciparum, C. perfringens, and Candida spp.

2. Materials and Methods

2.1. Case Presentation

On October 29th 2005, a 56-year-old German tourist living in Haiti, with a history of heavy alcohol use and 2 malaria infections treated with chloroquine, developed symptoms of fever, headache, nausea, and diarrhea. On November 3rd he visited a local hospital in Côtes des Arcadins and was diagnosed with P. falciparum infection by peripheral blood smear. The patient was treated with chloroquine and doxycycline the same day but developed altered mental status and was hospitalized. Despite falling parasite counts, the patient’s neurological condition continued to worsen and he was mechanically ventilated. Seizures, bloody stools, hematemesis, and decreased urinary output were also documented. Due to his worsening condition, he was transferred to a hospital in Miami the following day, November 4th. At the time of hospital admission in Miami, the patient had thrombocytopenia, diffuse intravascular coagulation, electrolyte imbalance, and acute renal failure. Blood smears showed few malaria parasites, but treatment with antimalarial agents was continued. Bronchoalveolar lavage was positive for Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomas aeruginosa, and yeast forms.

Blood culture on November 4th was positive for C. perfringens. Vancomycin, amphotericin, piperacillin, phenytoin, lorazepam, and hydrocortisone were added to the treatment regimen. On November 5th blood culture revealed Candida tropicalis. An encephalitis panel was also negative. The patient continued to decline clinically and he expired on November 7th, 10 days after symptom onset.

2.2. Tissue Samples and Immunohistochemical Analyses

Formalin-fixed, paraffin-embedded tissue (FFPET) sections of trachea, lung, heart, liver, spleen, kidney, small intestine, and central nervous system (CNS) were submitted to the Infectious Diseases Pathology Branch (IDPB) at the Centers for Disease Control and Prevention for diagnostic consultation.

Tissue sections were evaluated by routine hematoxylin and eosin (H&E), GMS, gram and Steiner stains, and were subsequently tested by immunohistochemistry (IHC) for suspected pathogens using immunoalkaline phosphatase technique as described previously [15, 16]. In brief, FFPET sections were deparaffinized in xylene and rehydrated in a graded alcohol series. IHC pretreatment conditions varied by primary antibody, and as deemed appropriate, consisted of one of the following 2 methods. (1) Antigen retrieval was performed by incubating sections submerged in Antigen Retrieval Citra Solution (BioGenex, San Ramon, Calif, USA) in a steamer for 10 minutes or (2) sections were digested in 0.1 mg/mL proteinase K (Boehringer-Mannheim, Indianapolis, Ind, USA) solution for 15 minutes. Sections were then blocked with 20% normal sheep serum in Tris-saline-Triton (NSS/TST) and incubated with the primary antibody (see below) for 60 minutes on the autostainer (DAKO, Carpinteria, Calif, USA). Detection of the bound antibody was performed using a secondary biotinylated antimouse antibody (DAKO), alkaline phosphatase-conjugated streptavidin, and naphthol phosphatase-fast red chromogen reagent. Slides were rinsed, counterstained in Mayer’s hematoxylin, and mounted with aqueous mounting medium.

The primary antibodies used in immunohistochemical assays included P. falciparum histidine rich protein-2 (HRP-2, Biodesign, Saco, Maine, dilution 1:1000), a protein only produced by P. falciparum [16]; a polyclonal antibody reactive with various Clostridium species including C. perfringens, C. botulinum, C. sordelii, C. novyii, and C. subterminale (Biodesign, dilution 1:1000) [15]; a polyclonal antibody reactive with Candida species (Meridian Life Sciences; dilution 1:200). Appropriate positive and negative controls were run in parallel.

2.3. Molecular Analyses

DNA was extracted from FFPET sections of small intestine using the QIAamp DNA minikit (Qiagen, Valencia, Calif, USA), following the tissue extraction protocol. A C. perfringens-specific PCR assay was performed using the High Fidelity PCR kit (Roche Diagnostics, Indianapolis, Ind, USA) according to the manufacturer’s instructions to amplify 283-bp fragment of the phospholipase C (alpha toxin) gene. For further evaluation, two P. falciparum- specific PCR assays targeting the 18S rRNA gene were performed. Primers used in PCR assays were published previously [17, 18] and are described in Table 1. PCR assays were modified for the FFPET. For each primer set, annealing temperature was adjusted accordingly. PCR was carried out on a GeneAmp PCR System 9700 thermocycler (Perkin-Elmer).

Primer sequence ( )Gene targetProduct size (bp)Anneling temperature ( )Reference

Clostridium perfringens specific PCR
PL3 AAG TTA CCT TTG CTG CAT AAT CCCPhospholipase C28355Fach and Popoff 1997 [17]

Plasmodium falciparum specific PCR
rFAL1 TTA AAC TGG TTT GGG AAA ACC AAA TAT ATT18S rRNA20558Perandin et al. 2004 [18]
FAL-F CTT TTG AGA GGT TTT GTT ACT TTG AGT AA18S rRNA9858Perandin et al. 2004 [18]

Amplified PCR products were separated on 1.8% agarose gel, extracted from the gel by using QIAquick gel extraction kit (Qiagen), and cycle sequenced by CEQ 2000 dye terminator cycle sequencing with quick start kit (Beckman Coulter, Fullerton, Calif, USA) and the respective primers. Postreaction cleanup was done by centri-sep spin columns (Princeton Separations, Adelphia, NJ). The samples were sequenced on a CEQ 2000 XL sequencer (Beckman Coulter, Fullerton, Calif, USA). Search for homologies to known sequences was done using the nucleotide database of the Basic Local Alignment Search Tool (BLAST) at

3. Results

No hemozoin pigment was observed by routine hematoxylin-eosin (H&E) stain and no malaria parasites were seen in red blood cells on careful examination of multiple tissues. Histopathology of the colon and small intestine mucosa showed extensive necrosis with diffuse, extensive, submucosal edema and multifocal inflammatory cell infiltrates comprised predominately of neutrophils (Figure 1(a)). The serosa was moderately thickened and contained mixed inflammatory cell infiltrates. The liver showed autolysis with no significant inflammatory cell infiltrates. Spleen sections were congested and necrotic. The mucosal surface of the larynx was also extensively necrotic with abundant neutrophilic infiltrates. There were diffuse autolysis in the kidneys and intra-alveolar edema in the lungs. The heart showed interstitial edema. There were focal hemorrhages in the white matter of the cerebral cortex, but no conspicuous inflammatory cell infiltrates observed in the hippocampus, pons, cerebellum, and spinal cord.

The HRP-2 IHC assay revealed discrete immunostaining of intra-erythrocytic parasites in CNS, kidney, liver, heart, and spleen (Figure 1(c)). HRP-2 antigens were also detected in endothelium of systemic and CNS blood vessels (Figure 1(d)), and in renal tubular epithelium and renal casts. The Clostridia spp. IHC assay revealed abundant immunostaining in necrotic areas of the small intestine (Figure 1(b)); other tissues were negative. Small budding yeasts in the alveolar space of the lung were identified by an IHC stain for Candida spp.

Amplification products of expected sizes were generated by both the C. perfringens and P.falciparum PCR assays using DNA extracted from FFPET sections. Sequence analysis of positive amplicons also confirmed the infections of P. falciparum and C. perfringens.

4. Discussion

Immunohistochemical and molecular analysis of FFPET sections from the study patient confirmed coinfections with P. falciparum, C. perfringens, and Candidia spp. Malaria is one of the most common causes of fever in travelers [19] and nosocomial coinfections may occur with a frequency of 25%, according to a recent study of 96 fatal P. falciparum cases [20]. However, malaria coinfections are difficult to diagnose clinically and may only be suspected when a patient fails to respond to malaria treatment [10]. Several observations suggest that the patient described here, who presented to hospital with classic malaria symptoms, was successfully treated for malaria infection with chloroquine and doxycycline: (1) declining parasite counts on peripheral blood smear were documented during his hospital stay; (2) absence of hemozoin, a birefringent pigment produced by plasmodium in correlation with parasite density [21, 22], on H&E evaluation; (3) rare HRP-2 antigens detected by IHC in CNS, heart, lung, and liver sections as described in detail above. Rare staining was anticipated in this patient, considering that HRP-2 antigens are slow to clear from the blood and may persist in treated patients for up to two weeks [23]. The presence of amplification products of P. falciparum using PCR assays is not inconsistent with the H&E and immunohistochemical findings of resolving malaria infection. The primers used are highly sensitive, shown to detect as few as 0.7 parasites/mL [18]. In this context, and as our patient illustrates, PCR results must be correlated with the patient’s clinical history.

The observation of necrosis in the small intestine supports the finding of C. perfringens in blood cultures found on November 4th, (day 7 of illness) after the patient was hospitalized in Miami. C. perfringens infection was subsequently confirmed by IHC testing and by PCR and sequencing analysis. C. perfringens is associated with several human diseases, including necrotizing enterocolitis [24], gas gangrene [25], antibiotic-associated diarrhea, and food poisoning outbreaks worldwide [26]. The alpha toxin is the most virulent of the 12 toxins produced by C. perfringens [9] because it destroys cell membranes, including those of red blood cells, platelets, and muscles. The bacterium also has sphingomyelinase activity that causes damage to the nerve-sheath in the central nervous system [8]. Deaths due to C. perfringens infections are rare in humans, and the portals of entry are usually surgical wounds [27]. However concomitant ischemia, or low oxygen tension in necrotic tissue, is a trigger for bacterial spore germination [28], and subsequent toxin production leads to anaerobic cellulitis or myonecrosis (gas gangrene) that rapidly progresses to severe sepsis [8]. The source of this patient’s C. perfringens infection is unknown as C. perfringens is widespread in the environment and can be a component of normal human flora, but broad spectrum antibiotic use is suspected. It is likely that P. falciparum infection increased susceptibility to C. perfringens and Candidaspp. in this patient.

C. perfringens infection causing intestinal myonecrosis may have begun with tissue ischemia due to P. falciparum sequestration, which is characterized by the attachment of parasitized erythrocytes (pRBCs) to endothelial cells lining blood vessels via a variety of constitutive receptors. Sequestration causes sluggish blood flow and disruption of microcirculation [6, 29] leading to ischemia. The infection subsequently leads to hyperlactemia, hypoglycemia, and metabolic acidosis, creating a dependence on anaerobic glycolysis for energy production [30]. Studies suggest that obstruction of the splanchnic blood vessels by pRBCs facilitates the entry of endotoxins and bacteria like C. perfringens from the digestive tract into the bloodstream [31]. While limited clinical data on this patient is available, this mechanism seems plausible and is supported by the tissue-based and molecular testing performed.

This patient’s chronic alcohol consumption may also have contributed to the severity of multiple infections. Ethanol has been shown to decrease the respiratory burst activity of neutrophils [32], and heavy alcohol consumption (> or = 5 drinks per day) is significantly associated with ICU-acquired bacterial infection, even when controlling for duration of mechanical ventilation and other risk factors [33]. Further, the oral flora of heavy alcohol drinkers has been shown to differ significantly from the flora of nonalcoholics. One study showed that anaerobes, including Clostridrium spp., are present in 84.5% of heavy drinkers, compared with 30.5% of nonalcoholics and similarly, Candida spp. were found in 34.5% of heavy drinkers whereas only 5.5% of nonalcoholics carried the microbiota [34]. The pathogens detected by bronchoalveolar lavage, Klebsiella pneumoniae, and Acinetobacter baumannii are particularly common causes of pneumonia in chronic alcoholics; while Pseudomas aeruginosa is associated with mechanical ventilation [35].

Disseminated candidiasis contributed to our patient’s demise; C. tropicalis was detected by bronchoalveolar lavage, and our IHC analysis revealed Candida spp. in FFPET of small intestine. Animal studies have shown that mucosal damage and broad-spectrum antibiotics are important factors in opportunistic candidiasis [30]. In this case, we suggest that the use of broad spectrum antibiotic coverage in the setting of tissue ischemia and mucosal erosion secondary to P. falciparum and C. perfringens infections facilitated disseminated infection.

To our knowledge, this is the first report of P. falciparum, C. perfringens, and Candida spp. coinfections. In the case presented here, P. falciparum may have increased susceptibility to C. perfringens infection by inducing a state of hypoxia-ischemia. The patient’s chronic alcohol consumption may have increased his susceptibility to intestinal necrosis and ischemia, which created a suitable environment for translocation and dissemination of Candida spp., particularly in the setting of broad-spectrum antibiotic administration. P.falciparum remains a significant threat to travelers to Haiti and other areas where the parasite is endemic. This case highlights the importance of suspecting bacterial and fungal coinfections in patients refractory to malaria treatment.


Authors thank the members of the Infectious Disease Pathology Branch, the Emerging Infectious Diseases Fellowship from the Association of Public Health Laboratories and the Oak Ridge Institute for Science and Education for making this work possible. This research was supported in part by an Emerging Infectious Diseases Fellowship from the Association of Public Health Laboratories and by an appointment to the Research Participation Program at the Centers for Disease Control and Prevention, National Center for Infectious Diseases, Infectious Disease Pathology Activity, by the Oak Ridge Institute for Science and Education through an interagency agreement between the U.S. Department of Energy and CDC.


  1. T. P. Eisele, J. Keating, A. Bennett et al., “Prevalence of Plasmodium falciparum infection in rainy season, Artibonite Valley, Haiti, 2006,” Emerging Infectious Diseases, vol. 13, no. 10, pp. 1494–1496, 2007. View at: Google Scholar
  2. “Severe falciparum malaria. World Health Organization, Communicable Diseases Cluster,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 94, pp. S1–S90, 2000. View at: Google Scholar
  3. World Malaria Report 2008, The World Health Organization. WHO Global Malaria Programme, March 2009,
  4. J. Thwing, J. Skarbinski, R. D. Newman et al., “Malaria surveillance-United States,” MMWR: Surveillance Summaries, vol. 56, no. 6, pp. 23–40, 2007. View at: Google Scholar
  5. I. W. Sherman, S. Eda, and E. Winograd, “Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind,” Microbes and Infection, vol. 5, no. 10, pp. 897–909, 2003. View at: Publisher Site | Google Scholar
  6. B. M. Cooke, S. Morris-Jones, B. M. Greenwood, and G. B. Nash, “Mechanisms of cytoadhesion of flowing, parasitized red blood cells from Gambian children with falciparum malaria,” American Journal of Tropical Medicine and Hygiene, vol. 53, no. 1, pp. 29–35, 1995. View at: Google Scholar
  7. R. S. Cotran, V. Kumar, and S. L. Robbins, Robbins Pathologic Basis of Disease, W.B. Saunders Company, Philadelphia, Pa, USA, 1994.
  8. J. Sakurai, M. Nagahama, and M. Oda, “Clostridium perfringens alpha-toxin: characterization and mode of action,” Journal of Biochemistry, vol. 136, no. 5, pp. 569–574, 2004. View at: Publisher Site | Google Scholar
  9. S. Inoue, J. A. Wirman, J. W. Alexander, O. Trocki, and R. R. Cardell, “Candida albicans translocation across the gut mucosa following burn injury,” Journal of Surgical Research, vol. 44, no. 5, pp. 479–492, 1988. View at: Publisher Site | Google Scholar
  10. F. Bruneel, B. Gachot, J. F. Timsit et al., “Shock complicating severe falciparum malaria in European adults,” Intensive Care Medicine, vol. 23, no. 6, pp. 698–701, 1997. View at: Publisher Site | Google Scholar
  11. R. Gopinath, J. S. Keystone, and K. C. Kain, “Concurrent falciparum malaria and salmonella bacteremia in travelers: report of two cases,” Clinical Infectious Diseases, vol. 20, no. 3, pp. 706–708, 1995. View at: Google Scholar
  12. P. Brouqui, J. M. Rolain, C. Foucault, and D. Raoult, “Short report: Q fever and Plasmodium falciparum malaria co-infection in a patient returning from the comoros archipelago,” American Journal of Tropical Medicine and Hygiene, vol. 73, no. 6, pp. 1028–1030, 2005. View at: Google Scholar
  13. S. Badiaga, G. Imbert, B. La Scola, P. Jean, J. Delmont, and P. Brouqui, “Imported brucellosis associated with Plasmodium falciparum malaria in a traveler returning from the tropics,” Journal of Travel Medicine, vol. 12, no. 5, pp. 282–284, 2005. View at: Google Scholar
  14. C. Wongsrichanalai, C. K. Murray, M. Gray et al., “Co-infection with malaria and leptospirosis,” American Journal of Tropical Medicine and Hygiene, vol. 68, no. 5, pp. 583–585, 2003. View at: Google Scholar
  15. G. L. Genrich, J. Guarner, C. D. Paddock et al., “Fatal malaria infection in travelers: novel immunohistochemical assays for the detection of Plasmodium falciparum in tissues and implications for pathogenesis,” American Journal of Tropical Medicine and Hygiene, vol. 76, no. 2, pp. 251–259, 2007. View at: Google Scholar
  16. J. Guarner, J. Bartlett, S. Reagan et al., “Immunohistochemical evidence of Clostridium sp, Staphylococcus aureus, and group A Streptococcus in severe soft tissue infections related to injection drug use,” Human Pathology, vol. 37, no. 11, pp. 1482–1488, 2006. View at: Publisher Site | Google Scholar
  17. P. Fach and M. R. Popoff, “Detection of enterotoxigenic Clostridium perfringens in food and fecal samples with a duplex PCR and the slide latex agglutination test,” Applied and Environmental Microbiology, vol. 63, no. 11, pp. 4232–4236, 1997. View at: Google Scholar
  18. F. Perandin, N. Manca, A. Calderaro et al., “Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis,” Journal of Clinical Microbiology, vol. 42, no. 3, pp. 1214–1219, 2004. View at: Publisher Site | Google Scholar
  19. P. Schlagenhauf and P. Muentener, “Imported malaria,” in Traveler's Malaria, P. Schlagenhauf, Ed., pp. 495–508, Decker, Hamilton, UK, 2001. View at: Google Scholar
  20. F. Legros, O. Bouchaud, T. Ancelle et al., “Risk factors for imported fatal Plasmodium falciparum malaria, France, 1996–2003,” Emerging Infectious Diseases, vol. 13, no. 6, pp. 883–888, 2007. View at: Google Scholar
  21. A. D. Sullivan, I. Ittarat, and S. R. Meshnick, “Patterns of haemozoin accumulation in tissue,” Parasitology, vol. 112, no. 3, pp. 285–294, 1996. View at: Google Scholar
  22. A. U. Orjih and C. D. Fitch, “Hemozoin production by Plasmodium falciparum: variation with strain and exposure to chloroquine,” Biochimica et Biophysica Acta, vol. 1157, no. 3, pp. 270–274, 1993. View at: Publisher Site | Google Scholar
  23. M. Mayxay, S. Pukrittayakamee, K. Chotivanich, S. Looareesuwan, and N. J. White, “Persistence of Plasmodium falciparum HRP-2 in successfully treated acute falciparum malaria,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 95, no. 2, pp. 179–182, 2001. View at: Publisher Site | Google Scholar
  24. J. Sobel, C. G. Mixter, P. Kolhe et al., “Necrotizing enterocolitis associated with Clostridium perfringens type A in previously healthy north american adults,” Journal of the American College of Surgeons, vol. 201, no. 1, pp. 48–56, 2005. View at: Publisher Site | Google Scholar
  25. S. Kuroda, Y. Okada, M. Mita et al., “Fulminant massive gas gangrene caused by Clostridium perfringens,” Internal Medicine, vol. 44, no. 5, pp. 499–502, 2005. View at: Publisher Site | Google Scholar
  26. S. G. Sparks, R. J. Carman, M. R. Sarker, and B. A. McClane, “Genotyping of enterotoxigenic Clostridium perfringens fecal isolates associated with antibiotic-associated diarrhea and food poisoning in North America,” Journal of Clinical Microbiology, vol. 39, no. 3, pp. 883–888, 2001. View at: Publisher Site | Google Scholar
  27. E. S. Caplan and R. M. Kluge, “Gas gangrene: review of 34 cases,” Archives of Internal Medicine, vol. 136, no. 7, pp. 788–791, 1976. View at: Publisher Site | Google Scholar
  28. C. R. Hitchcock, F. J. Demello, and J. J. Haglin, “Gangrene infection: new approaches to an old disease,” Surgical Clinics of North America, vol. 55, no. 6, pp. 1403–1410, 1975. View at: Google Scholar
  29. A. M. Dondorp, “Clinical significance of sequestration in adults with severe malaria,” Transfusion Clinique et Biologique, vol. 15, no. 1-2, pp. 56–57, 2008. View at: Publisher Site | Google Scholar
  30. N. J. White and M. Ho, “The pathophysiology of malaria,” Advances in Parasitology, vol. 31, pp. 83–173, 1992. View at: Publisher Site | Google Scholar
  31. I. A. Clark and W. B. Cowden, “The pathophysiology of falciparum malaria,” Pharmacology and Therapeutics, vol. 99, no. 2, pp. 221–260, 2003. View at: Publisher Site | Google Scholar
  32. D. Breitmeier, N. Becker, C. Weilbach et al., “Ethanol-induced malfunction of neutrophils respiratory burst on patients suffering from alcohol dependence,” Alcoholism: Clinical and Experimental Research, vol. 32, no. 10, pp. 1708–1713, 2008. View at: Publisher Site | Google Scholar
  33. A. Gacouin, F. Legay, C. Camus et al., “At-risk drinkers are at higher risk to acquire a bacterial infection during an intensive care unit stay than abstinent or moderate drinkers,” Critical care medicine, vol. 36, no. 6, pp. 1735–1741, 2008. View at: Publisher Site | Google Scholar
  34. V. Golin, I. M. Mimica, and L. M. Mimica, “Oropharynx microbiota among alcoholics and non-alcoholics,” São Paulo Medical Journal, vol. 116, no. 3, pp. 1727–1733, 1998. View at: Google Scholar
  35. E. Bergogne-Bérézin, “Pseudomonads and miscellaneous gram-negative bacilli,” in Infectious Diseases, J Cohen and W. G. Powderly, Eds., pp. 2203–2217, Mosby, St. Louis, Mo, USA, 2nd edition, 2004. View at: Google Scholar

Copyright © 2009 Gillian L. Genrich et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

More related articles

 PDF Download Citation Citation
 Download other formatsMore
 Order printed copiesOrder

Related articles

Article of the Year Award: Outstanding research contributions of 2020, as selected by our Chief Editors. Read the winning articles.