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Citrobacter frendii infections in humans and reptilians
History and diseases associated with the bacterium
First identified in 1932 by Wang, Chang, Chen, Luh, (2000) Citrobacter frendii is a facultative
anaerobic bacterium, measuring around 1-5 μm, which is gram-negative under the Gram-
straining method of bacterial differentiation. It is useful in the nitrogen cycle in the
environment, so is often used as a good producer of nitrate when around high levels of
ammonium ions in soil (Doran, 1999).
Belonging to the Enterobacteriaceae family (which comprises of other infective bacterium, such
as Salmonella, which is often found in similar reptilian hosts that are infected with the
bacterium), it is a highly prevalent amongst both human and animal hosts, causing diseases
such as pneumonia (Mateos Rodriguez, Perez Moro, Atienza Morales and Beato Perez, 2000;
Zuniga, Gonzalez, Henriquez and Fernandez, 1991), bloodstream infections (Tellez, Chrysant,
Omer and Dismukes, 2000), meningitis (Kline, 1988), urinary tract infections, neonatal sepsis,
brain abscess (Graham and Band, 1981; Kline, 1988) and intra-abdominal sepsis (Shih, Chen,
Chang, Luh and Hsieh, 1996) in humans.
Transmission
In humans, this bacterium is transmitted through a number of ways, mainly through person-to-
person transmission (often through fecal matter in infants) (Doran, 1999; Tschape, Prager,
Streckel, Fruth, Tietze and Bohme, 1995), and sometimes through an alternative tract, for
example through swine manure used to fertilise Parsley crops in Canada, which resulted in one
death and eight urinary tract infections, as stated in a report by Tschape, Prager, Streckel,
Fruth, Tietze and Bohme (1995).
As well as being present in humans, the bacterium is also often found in animal species such as
catfish (Nawaz, 2008) and reptiles, in particular turtles, terrapins and tortoises (Raidal, Ohara,
Hobbs and Prince, 1998).
With defecation in water and on land, the bacterium can easily be transmitted from one
reptilian host to another (D'Aoust, Daley, Crozier and Sewell, 1990) as they are known to
excrete a number of other bacterium such as Salmonella (Ebani, Cerri, Fratini, Meille, Valentini,
and Andreani, 2005). So, theoretically, most individuals of a closely living area could be infected
from just one host, especially ones of an aquatic lifecycle in an enclosed area such as a pond. In
addition to the bacterium being able to survive through the fecal matter, again, it can survive in
P a g e | 2
many areas such as soil, which could be accidentally ingested by an animal whilst grazing for
vegetation.
Current status of infections/how prevalent is it?
In an article by Chen, Wong, Fung, Yu and Liu (2002), between the years of 1996 to 1999 there
was 36 cases of treatment relating to the bacterium at a particular hospital in Taipei, with a
mortality rate of 22%. In addition, an article by Drelichman and Band (1985) showed 38 patients
with the Citrobacter infection between the years of 1974 to 1982 in “two adult community-
teaching hospitals in the Detroit Medical Center.” Overall, it seemed to develop with a 65%
likelihood in elderly patients and 77% acquired it through hospital transmission, with 48%
fatality of this study alone (Drelichman and Band, 1985).
From cloaca swabs of 39 captive red-eared sliders (Trachemys scripta elegans), 20 of these
individuals were found to have the Citrobacter bacterium in the samples, alongside many other
bacterium spp. (Gioia-Di Chiacchio, Penido, de Souza, Prioste, Prado, Knobl, Menao and
Matushima, 2014). However, further studies are needed, as the transmission between reptilian-
to-human transmission through handling due to the pet trade boom of the species will need to
be taken into account, as I suspect this number will be much higher overall for this species
especially (own knowledge of pet trade and herpetology). However, in a study by Benetka,
Grabensteiner, Gumpenberger, Neubauer, Hirschmuller and Mostl (2007), found that some
species recovered after merely four months of an infection, so it is possible that the individuals
can recover or become re-infected along the course of time.
Current approaches to the infection
In human and reptilian approaches, currently antimicrobial agents are used to treat patients
with a positive sign of the bacterium infection. Success seems to be with bleach, chlorohexidine
detergent scrub (Rutala and Weber, 1997), hexachlorophene or iodophor preparations (Public
Health Agency of Canada, 2004), Ethanol (0.41M) (Ojajärvi, 1980), “Phenolic disinfectants, 1%
sodium hypochlorite, 70% ethanol, formaldehyde, glutaraldehyde, iodophore and paracetic
acid” (Collins and Kennedy, 1999).
However, the Citrobacter infection has built up a resistance to some treatments, such as
carbenicillin, cephalothin (Abbott, 2007), ampicillin (Doran, 1999), ceftazidime,
antipseudomona penicillins, cephalosporins and piperacillintazobactam (Lavigne, Defez,
Bouziges, Mahamat and Sotto, 2007).
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With reptiles in particular, povidone-iodine or chlorhexidine solution scrub is the most
commonly used treatment for minor infections, with only the severe infections requiring
antibiotic treatment. From a personal experience, I have cared for two species, a yellow-bellied
slider (Trachemys scripta scripta) and a Cumberland slider (Trachemys scripta troostii) who
tested positive for signs of Citrobacter when they came into my care in November 2014, Figures
1-4 show progression through antimicrobial scrub treatment of the yellow-bellied slider, with
Figure 1 showing initial signs of infection, commonly displayed through “Shell rot.”
Figure 1 - Cumberland slider displaying signs of "shell rot" caused by the bacterium, November 2014
Figure 2 - Cumberland slider (left) and yellow-belled slider (right) showing signs of "shell rot" through flaking scutes and severe
discolouration in areas of the shell. December 2014
Figure 3 - Yellow-bellied slider showing signs of improvement through treatment, dated January 2015
P a g e | 4
Figure 4 - Cumberland slider showing vast improvement through antimicrobial cleansing treatment, dated January 2015
Bibliography
Abbott, S. L. (2007). Klebsiella, Enterobacter, Citrobacter, Serratia, Plesiomonas, and Other Enterobacteriaceae. In
P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller & M. L. Landry (Eds.), Manual of Clinical Microbiology (9 th
ed., pp. 698-715). Washington, DC: ASM press.
Benetka, V., Grabensteiner, E., Gumpenberger, M., Neubauer, C., Hirschmuller, B., Mostl, K.. (2007). First report of
an iridovirus (Genus Ranavirus) infection in a Leopard tortoise (Geochelone pardalis pardalis). WIENER
TIERARZTLICHE MONATSSCHRIFT. 94 (9-10), Pages 243-248.
Chen S. Y., Wong, W. W., Fung P. C., Yu W. K., Liu Y. C. (2002). Clinical features and antimicrobial susceptibility
trends in Citrobacter freundii bacteremia.. Journal of Microbiology, Immunology, and Infection. 35 (2), Pages 109-
114.
P a g e | 5
Collins, C. H., Kennedy, D. A. (1999). Decontamination. Laboratory-Acquired Infections: History, Incidence, Causes
and Prevention. (4th ed., pp. 160-186). London, UK: Buttersworth.
D'Aoust, J. Y., Daley, E., Crozier, M., Sewell, M. A. (1990). Pet turtles: a continuing international threat to public
health. Am. J. Epidemiol. 132:233-238.
Doran, T. I. (1999). The role of Citrobacter in clinical disease of children: Review. Clinical Infectious Diseases, 28(2),
Pages 384-394.
Drelichman, V., Band, D. J.. (1985). Bacteremias due to Citrobacter diversus and Citrobacter freundiiIncidence, Risk
Factors, and Clinical Outcome. Arch Intern Med.. 145 (10), Pages 1808-1810.
Ebani, V. V., Cerri, D., Fratini, F., Meille, N., Valentini, P., Andreani, E. (2005). Salmonella enterica isolates from
faeces of domestic reptiles and a study of their antimicrobial in vitro sensitivity. Res. Vet. Sci. 78:117-121.
Gioia-Di Chiacchio, R., Penido, N. G., de Souza, CAI., Prioste, FES., Prado, S. M., Knobl, T., Menao, C. M., Matushima,
R. E.. (2014). ENTEROBACTERIAL COLONIZATION IN CAPTIVE RED-EARED SLIDERS (TRACHEMYS SCRIPTA ELEGANS).
JOURNAL OF ZOO AND WILDLIFE MEDICINE. 45 (4), Pages 919-921.
Graham, D. R., Band, D. J. (1981). Citrobacter diversus brain abscess and meningitis in neonates. JAMA 245:1923-
1925.
Kline, M. W. (1988). Citrobacter meningitis and brain abscess in infancy: epidemiology, pathogenesis, and
treatment. J. Pediatr. 113:430-434.
Lavigne, J. P., Defez, C., Bouziges, N., Mahamat, S., Sotto, A. (2007). Clinical and molecular epidemiology of
multidrug-resistant Citrobacter spp. infections in a French university hospital. Eur J Clin Microbiol Infect Dis, 26,
Pages 439-441.
Mateos Rodriguez, F., Perez Moro, E., Atienza Morales, P. M., Beato Perez. L. J. (2000). Community-acquired
bacteremic pneumonia due to Citrobacter diversus. An. Med. Int. 17:165-166.
Nawaz, M. (2008). Isolation and characterization of tetracycline-resistant Citrobacter spp. from catfish. Food
Microbiol., 25(1), Pages 85-91.
Ojajärvi, J. (1980). Effectiveness of hand washing and disinfection methods in removing transient bacteria after
patient nursing. J Hyg (Lond)., 85(2), Pages193-203.
Pepperell, C., Kus, J. V., Gardam, M. A., Humar, A., & Burrows, L. L. (2002). Low-Virulence Citrobacter Species
Encode Resistance to Multiple Antimicrobials. Antimicrob. Agents Chemother., Nov.,46(11), Pages 3555-3560.
Public Health Agency of Canada. (2004). In Best M., Graham M. L., Leitner R., Ouellette M. and Ugwu K. (Eds.),
Laboratory Biosafety Guidelines (3rd ed.). Canada: Public Health Agency of Canada.
Raidal, R. S., Ohara, M., Hobbs, P. R., Prince, I. R. (1998). Gram-negative bacterial infections and cardiovascular
parasitism in green sea turtles (Chelonia mydas). Australian Veterinary Journal. 76 (6), Pages 415-7.
Rutala, W., & Weber, D. (1997). Uses of inorganic hypochlorite (bleach) in health-care facilities. Clinical
Microbiology Reviews, 10(4), Pages 597-610.
P a g e | 6
Shih, C. C., Chen, Y. C., Chang, C. S., Luh, T. K., Hsieh, C. W. (1996). Bacteremia due to Citrobacter species:
significance of primary intra-abdominal infection. Clin. Infect. Dis. 23:543-549.
Tschape, H., Prager, R., Streckel, W., Fruth, A., Tietze, E., & Bohme, G. (1995). Verotoxinogenic Citrobacter freundii
associated with severe gastroenteritis and cases of haemolytic uraemic syndrome in a nursery school: green butter
as the infection source. Epidemiology and Infection, 114(3), Pages 441-450.
Tellez, I., Chrysant, S. G., Omer, I, Dismukes, E. W., (2000). Citrobacter diversus endocarditis. Am. J. Med. Sci.
320:408-410.
Wang T. J., Chang C. S., Chen C. Y., Luh T. K. (2000). Comparison of antimicrobial susceptibility of Citrobacter
freundii isolates in two different time periods. . Journal of Microbiology, Immunology, and Infection. 33 (4), Pages
258-262.
Zuniga, J., Gonzalez, P., Henriquez, A., Fernandez, A. (1991). Bacteremic pneumonia caused by Citrobacter diversus:
report of a case. Rev. Med. Chile 119:303-307.
P a g e | 6
Shih, C. C., Chen, Y. C., Chang, C. S., Luh, T. K., Hsieh, C. W. (1996). Bacteremia due to Citrobacter species:
significance of primary intra-abdominal infection. Clin. Infect. Dis. 23:543-549.
Tschape, H., Prager, R., Streckel, W., Fruth, A., Tietze, E., & Bohme, G. (1995). Verotoxinogenic Citrobacter freundii
associated with severe gastroenteritis and cases of haemolytic uraemic syndrome in a nursery school: green butter
as the infection source. Epidemiology and Infection, 114(3), Pages 441-450.
Tellez, I., Chrysant, S. G., Omer, I, Dismukes, E. W., (2000). Citrobacter diversus endocarditis. Am. J. Med. Sci.
320:408-410.
Wang T. J., Chang C. S., Chen C. Y., Luh T. K. (2000). Comparison of antimicrobial susceptibility of Citrobacter
freundii isolates in two different time periods. . Journal of Microbiology, Immunology, and Infection. 33 (4), Pages
258-262.
Zuniga, J., Gonzalez, P., Henriquez, A., Fernandez, A. (1991). Bacteremic pneumonia caused by Citrobacter diversus:
report of a case. Rev. Med. Chile 119:303-307.

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Biology and Control of Vertebrate Pests.pdf
 

Citrobacter frendii infections in Reptiles

  • 1. P a g e | 1 Citrobacter frendii infections in humans and reptilians History and diseases associated with the bacterium First identified in 1932 by Wang, Chang, Chen, Luh, (2000) Citrobacter frendii is a facultative anaerobic bacterium, measuring around 1-5 μm, which is gram-negative under the Gram- straining method of bacterial differentiation. It is useful in the nitrogen cycle in the environment, so is often used as a good producer of nitrate when around high levels of ammonium ions in soil (Doran, 1999). Belonging to the Enterobacteriaceae family (which comprises of other infective bacterium, such as Salmonella, which is often found in similar reptilian hosts that are infected with the bacterium), it is a highly prevalent amongst both human and animal hosts, causing diseases such as pneumonia (Mateos Rodriguez, Perez Moro, Atienza Morales and Beato Perez, 2000; Zuniga, Gonzalez, Henriquez and Fernandez, 1991), bloodstream infections (Tellez, Chrysant, Omer and Dismukes, 2000), meningitis (Kline, 1988), urinary tract infections, neonatal sepsis, brain abscess (Graham and Band, 1981; Kline, 1988) and intra-abdominal sepsis (Shih, Chen, Chang, Luh and Hsieh, 1996) in humans. Transmission In humans, this bacterium is transmitted through a number of ways, mainly through person-to- person transmission (often through fecal matter in infants) (Doran, 1999; Tschape, Prager, Streckel, Fruth, Tietze and Bohme, 1995), and sometimes through an alternative tract, for example through swine manure used to fertilise Parsley crops in Canada, which resulted in one death and eight urinary tract infections, as stated in a report by Tschape, Prager, Streckel, Fruth, Tietze and Bohme (1995). As well as being present in humans, the bacterium is also often found in animal species such as catfish (Nawaz, 2008) and reptiles, in particular turtles, terrapins and tortoises (Raidal, Ohara, Hobbs and Prince, 1998). With defecation in water and on land, the bacterium can easily be transmitted from one reptilian host to another (D'Aoust, Daley, Crozier and Sewell, 1990) as they are known to excrete a number of other bacterium such as Salmonella (Ebani, Cerri, Fratini, Meille, Valentini, and Andreani, 2005). So, theoretically, most individuals of a closely living area could be infected from just one host, especially ones of an aquatic lifecycle in an enclosed area such as a pond. In addition to the bacterium being able to survive through the fecal matter, again, it can survive in
  • 2. P a g e | 2 many areas such as soil, which could be accidentally ingested by an animal whilst grazing for vegetation. Current status of infections/how prevalent is it? In an article by Chen, Wong, Fung, Yu and Liu (2002), between the years of 1996 to 1999 there was 36 cases of treatment relating to the bacterium at a particular hospital in Taipei, with a mortality rate of 22%. In addition, an article by Drelichman and Band (1985) showed 38 patients with the Citrobacter infection between the years of 1974 to 1982 in “two adult community- teaching hospitals in the Detroit Medical Center.” Overall, it seemed to develop with a 65% likelihood in elderly patients and 77% acquired it through hospital transmission, with 48% fatality of this study alone (Drelichman and Band, 1985). From cloaca swabs of 39 captive red-eared sliders (Trachemys scripta elegans), 20 of these individuals were found to have the Citrobacter bacterium in the samples, alongside many other bacterium spp. (Gioia-Di Chiacchio, Penido, de Souza, Prioste, Prado, Knobl, Menao and Matushima, 2014). However, further studies are needed, as the transmission between reptilian- to-human transmission through handling due to the pet trade boom of the species will need to be taken into account, as I suspect this number will be much higher overall for this species especially (own knowledge of pet trade and herpetology). However, in a study by Benetka, Grabensteiner, Gumpenberger, Neubauer, Hirschmuller and Mostl (2007), found that some species recovered after merely four months of an infection, so it is possible that the individuals can recover or become re-infected along the course of time. Current approaches to the infection In human and reptilian approaches, currently antimicrobial agents are used to treat patients with a positive sign of the bacterium infection. Success seems to be with bleach, chlorohexidine detergent scrub (Rutala and Weber, 1997), hexachlorophene or iodophor preparations (Public Health Agency of Canada, 2004), Ethanol (0.41M) (Ojajärvi, 1980), “Phenolic disinfectants, 1% sodium hypochlorite, 70% ethanol, formaldehyde, glutaraldehyde, iodophore and paracetic acid” (Collins and Kennedy, 1999). However, the Citrobacter infection has built up a resistance to some treatments, such as carbenicillin, cephalothin (Abbott, 2007), ampicillin (Doran, 1999), ceftazidime, antipseudomona penicillins, cephalosporins and piperacillintazobactam (Lavigne, Defez, Bouziges, Mahamat and Sotto, 2007).
  • 3. P a g e | 3 With reptiles in particular, povidone-iodine or chlorhexidine solution scrub is the most commonly used treatment for minor infections, with only the severe infections requiring antibiotic treatment. From a personal experience, I have cared for two species, a yellow-bellied slider (Trachemys scripta scripta) and a Cumberland slider (Trachemys scripta troostii) who tested positive for signs of Citrobacter when they came into my care in November 2014, Figures 1-4 show progression through antimicrobial scrub treatment of the yellow-bellied slider, with Figure 1 showing initial signs of infection, commonly displayed through “Shell rot.” Figure 1 - Cumberland slider displaying signs of "shell rot" caused by the bacterium, November 2014 Figure 2 - Cumberland slider (left) and yellow-belled slider (right) showing signs of "shell rot" through flaking scutes and severe discolouration in areas of the shell. December 2014 Figure 3 - Yellow-bellied slider showing signs of improvement through treatment, dated January 2015
  • 4. P a g e | 4 Figure 4 - Cumberland slider showing vast improvement through antimicrobial cleansing treatment, dated January 2015 Bibliography Abbott, S. L. (2007). Klebsiella, Enterobacter, Citrobacter, Serratia, Plesiomonas, and Other Enterobacteriaceae. In P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller & M. L. Landry (Eds.), Manual of Clinical Microbiology (9 th ed., pp. 698-715). Washington, DC: ASM press. Benetka, V., Grabensteiner, E., Gumpenberger, M., Neubauer, C., Hirschmuller, B., Mostl, K.. (2007). First report of an iridovirus (Genus Ranavirus) infection in a Leopard tortoise (Geochelone pardalis pardalis). WIENER TIERARZTLICHE MONATSSCHRIFT. 94 (9-10), Pages 243-248. Chen S. Y., Wong, W. W., Fung P. C., Yu W. K., Liu Y. C. (2002). Clinical features and antimicrobial susceptibility trends in Citrobacter freundii bacteremia.. Journal of Microbiology, Immunology, and Infection. 35 (2), Pages 109- 114.
  • 5. P a g e | 5 Collins, C. H., Kennedy, D. A. (1999). Decontamination. Laboratory-Acquired Infections: History, Incidence, Causes and Prevention. (4th ed., pp. 160-186). London, UK: Buttersworth. D'Aoust, J. Y., Daley, E., Crozier, M., Sewell, M. A. (1990). Pet turtles: a continuing international threat to public health. Am. J. Epidemiol. 132:233-238. Doran, T. I. (1999). The role of Citrobacter in clinical disease of children: Review. Clinical Infectious Diseases, 28(2), Pages 384-394. Drelichman, V., Band, D. J.. (1985). Bacteremias due to Citrobacter diversus and Citrobacter freundiiIncidence, Risk Factors, and Clinical Outcome. Arch Intern Med.. 145 (10), Pages 1808-1810. Ebani, V. V., Cerri, D., Fratini, F., Meille, N., Valentini, P., Andreani, E. (2005). Salmonella enterica isolates from faeces of domestic reptiles and a study of their antimicrobial in vitro sensitivity. Res. Vet. Sci. 78:117-121. Gioia-Di Chiacchio, R., Penido, N. G., de Souza, CAI., Prioste, FES., Prado, S. M., Knobl, T., Menao, C. M., Matushima, R. E.. (2014). ENTEROBACTERIAL COLONIZATION IN CAPTIVE RED-EARED SLIDERS (TRACHEMYS SCRIPTA ELEGANS). JOURNAL OF ZOO AND WILDLIFE MEDICINE. 45 (4), Pages 919-921. Graham, D. R., Band, D. J. (1981). Citrobacter diversus brain abscess and meningitis in neonates. JAMA 245:1923- 1925. Kline, M. W. (1988). Citrobacter meningitis and brain abscess in infancy: epidemiology, pathogenesis, and treatment. J. Pediatr. 113:430-434. Lavigne, J. P., Defez, C., Bouziges, N., Mahamat, S., Sotto, A. (2007). Clinical and molecular epidemiology of multidrug-resistant Citrobacter spp. infections in a French university hospital. Eur J Clin Microbiol Infect Dis, 26, Pages 439-441. Mateos Rodriguez, F., Perez Moro, E., Atienza Morales, P. M., Beato Perez. L. J. (2000). Community-acquired bacteremic pneumonia due to Citrobacter diversus. An. Med. Int. 17:165-166. Nawaz, M. (2008). Isolation and characterization of tetracycline-resistant Citrobacter spp. from catfish. Food Microbiol., 25(1), Pages 85-91. Ojajärvi, J. (1980). Effectiveness of hand washing and disinfection methods in removing transient bacteria after patient nursing. J Hyg (Lond)., 85(2), Pages193-203. Pepperell, C., Kus, J. V., Gardam, M. A., Humar, A., & Burrows, L. L. (2002). Low-Virulence Citrobacter Species Encode Resistance to Multiple Antimicrobials. Antimicrob. Agents Chemother., Nov.,46(11), Pages 3555-3560. Public Health Agency of Canada. (2004). In Best M., Graham M. L., Leitner R., Ouellette M. and Ugwu K. (Eds.), Laboratory Biosafety Guidelines (3rd ed.). Canada: Public Health Agency of Canada. Raidal, R. S., Ohara, M., Hobbs, P. R., Prince, I. R. (1998). Gram-negative bacterial infections and cardiovascular parasitism in green sea turtles (Chelonia mydas). Australian Veterinary Journal. 76 (6), Pages 415-7. Rutala, W., & Weber, D. (1997). Uses of inorganic hypochlorite (bleach) in health-care facilities. Clinical Microbiology Reviews, 10(4), Pages 597-610.
  • 6. P a g e | 6 Shih, C. C., Chen, Y. C., Chang, C. S., Luh, T. K., Hsieh, C. W. (1996). Bacteremia due to Citrobacter species: significance of primary intra-abdominal infection. Clin. Infect. Dis. 23:543-549. Tschape, H., Prager, R., Streckel, W., Fruth, A., Tietze, E., & Bohme, G. (1995). Verotoxinogenic Citrobacter freundii associated with severe gastroenteritis and cases of haemolytic uraemic syndrome in a nursery school: green butter as the infection source. Epidemiology and Infection, 114(3), Pages 441-450. Tellez, I., Chrysant, S. G., Omer, I, Dismukes, E. W., (2000). Citrobacter diversus endocarditis. Am. J. Med. Sci. 320:408-410. Wang T. J., Chang C. S., Chen C. Y., Luh T. K. (2000). Comparison of antimicrobial susceptibility of Citrobacter freundii isolates in two different time periods. . Journal of Microbiology, Immunology, and Infection. 33 (4), Pages 258-262. Zuniga, J., Gonzalez, P., Henriquez, A., Fernandez, A. (1991). Bacteremic pneumonia caused by Citrobacter diversus: report of a case. Rev. Med. Chile 119:303-307.
  • 7. P a g e | 6 Shih, C. C., Chen, Y. C., Chang, C. S., Luh, T. K., Hsieh, C. W. (1996). Bacteremia due to Citrobacter species: significance of primary intra-abdominal infection. Clin. Infect. Dis. 23:543-549. Tschape, H., Prager, R., Streckel, W., Fruth, A., Tietze, E., & Bohme, G. (1995). Verotoxinogenic Citrobacter freundii associated with severe gastroenteritis and cases of haemolytic uraemic syndrome in a nursery school: green butter as the infection source. Epidemiology and Infection, 114(3), Pages 441-450. Tellez, I., Chrysant, S. G., Omer, I, Dismukes, E. W., (2000). Citrobacter diversus endocarditis. Am. J. Med. Sci. 320:408-410. Wang T. J., Chang C. S., Chen C. Y., Luh T. K. (2000). Comparison of antimicrobial susceptibility of Citrobacter freundii isolates in two different time periods. . Journal of Microbiology, Immunology, and Infection. 33 (4), Pages 258-262. Zuniga, J., Gonzalez, P., Henriquez, A., Fernandez, A. (1991). Bacteremic pneumonia caused by Citrobacter diversus: report of a case. Rev. Med. Chile 119:303-307.