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Hemochromatosis, Iron, and Septicemia Caused by Vibrio vulnificus
Abstract
Vibrio vulnificus is killed by normal human blood but grows rapidly in blood from patients with hemochromatosis. It also grows in normal blood if the saturation of the transferrin is increased or if hematin, which contains iron, is added. It is suggested that the increased availability of iron in the blood of patients with chronic iron overload is responsible for their enhanced susceptibility to infection with V vulnificus.
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“Induction of hypoferremia, via systemic inhibition of extracellular Fe export coupled to increased Mø Fe/heme uptake and intracellular retention [5,6], reduces the growth and virulence of extracellular pathogens, as illustrated for Vibrio vulnificus infection in mice [96,97].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [97]
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“vulnificus infection [13-15], it remains unclear what role the iron overloaded state plays in human illness when liver disease is absent; this question deserves further study.”
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“Induction of hypoferremia, via systemic inhibition of extracellular Fe export coupled to increased Mø Fe/heme uptake and intracellular retention [5,6], reduces the growth and virulence of extracellular pathogens, as illustrated for Vibrio vulnificus infection in mice [96,97].”
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“The most decisive host factor required for in vivo growth of V. vulnificus has been reported to be iron (Chung et al., 1990; Bullen et al., 1991; Kraffert and Hogan, 1992; Starks et al., 2000).”
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“Thus, patients with hemochromatosis are highly susceptible to infections with Vibrio vulnificus, a bacterium that usually cannot grow in blood from healthy individuals, but rapidly grows in blood from patients with hemochromatosis (38).”
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“Do our findings have relevance for infectious disease in humans? Patients with type I (HFE mutation-associated) hemochromatosis are known to be susceptible to certain systemic bacterial infections, especially Vibrio vulnificus septicemia and hepatic abscesses caused by Yersinia enterocolitica [33, 34, 48, 49].”
BackgroundPhage Therapy of Local and Systemic Disease Caused by Vibrio vulnificus in Iron-Dextran-Treated Mice
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“…1 haemochromatosis Variations of Hfe Low macrophage iron Increased susceptibility to Yersinia enterocolitica and Vibrio vulnificus (Bullen et al. 1991; Doherty 2007; Gerhard et al. 2001) Minimal susceptibility to infections (Porto and de Sousa 2007) Mycobacterium tuberculosis…”
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“Vibrio vulnificus, a halophilic gram-negative marine bacterium, causes infectious diseases in humans, especially in people who are immunocompromised or have underlying conditions such as hemochromatosis, liver cirrhosis, or alcoholism (3, 4, 5, 29).”
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“Vibrio vulnificus, a gram-negative estuarine bacterium, causes wound infections and septicemia in humans, mostly in immunocompromised people and those with underlying conditions such as hemochromatosis, liver cirrhosis, and alcoholism (2, 3, 5, 23).”
BackgroundMechanism of High Susceptibility of Iron‐Overloaded Mouse to Vibrio vulnificus Infection
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“vulnificus subtype (various genetically distinct subgroups of biotype 1 identified by randomly amplified polymorphic DNA PCR appear to be especially virulent), immunocompromised state (human immunodeficiency virus, cancer, bone marrow suppression, achlorhydria, and diabetes), end-stage renal impairment, liver impairme…”
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“The organism lacks the ability to acquire iron from unsaturated ferritin and “likes” the free iron available in patients with liver disease [ 16 ].”
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“The mechanism underlying this effect and its potential relationship to stabilization of HIF-1a remain to be elucidated.Work from our laboratory has been directed at characterizing abnormalities of innate immunity in disorders of iron homeostasis. The results of our recent studies have indicated that macrophages from H…”
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“patients with underlying pathologies) septicaemia (Morris 1981; Bullen et al. 1991; Ardiç and Ozyurt 2004; McLaughlin et al. 2005; Oliver 2005).”
BackgroundLong-term follow-up after liver transplantation in patients with hepatic iron overload
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“V vulnificus is usually killed by normal human serum, but it grows rapidly when the iron-saturation level of transferrin is intentionally increased to >50% [16-18].”
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BackgroundAn Epimerase Gene Essential for Capsule Synthesis in Vibrio vulnificus
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“Capsule expression has been directly associated with virulence by mouse lethality studies (11, 47, 57) and transferrin-bound iron utilization (12, 33, 46).”
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Neutrophils from hereditary hemochromatosis patients are protected from iron excess and are primed
Renassia, C., Louis, S., Cuvellier, S., Boussetta, N., Deschemin, J., Borderie, D., Bailly, K., Poupon, J., Dang, P. M., Benna, J. E., et al. (2020) · Blood Advances · doi:10.1182/bloodadvances.2020002198 · Cited by 35
“Concerning HH, case reports have described an increased prevalence of certain infections with intracellular bacteria such as Yersinia enterocolitica,(50,51) Y pseudotuberculosis,(50,52) Listeria monocytogenes,(53) and Vibrio vulnificus.(54) These pathogens require higher iron concentrations for growth.”
BackgroundTransition Metal Homeostasis in Streptococcus pyogenes and Streptococcus pneumoniae
Turner, A. G., Ong, C. Y., Walker, M. J., Djoko, K. Y., & McEwan, A. G. (2017) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2017.01.002 · Cited by 35
Buck, E. D. J. D., Pauwels, N., Dieltjens, T., Compernolle, V., & Vandekerckhove, P. G. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2012.04.040 · Cited by 33
“…(I to V) and Yersinia enterocolitica (O:3, O:9 O:5.27) in serum samples hemochromatosis patients compared to control blood donors None Bullen et al., 1991 (United states) [49] In vitro study Five iron-overloaded hemochromatosis patients and five healthy people; patient…”
BackgroundInfluentialSayed, S. M. E., Abou‐Taleb, A., Nabo, M. M. H., Mahmoud, H. S., Ahmed, N. S., Baghdadi, H., & Mariah, R. (2014) · Journal of Blood Medicine · doi:10.2147/jbm.s65042 · Cited by 32
A functional defect in hereditary haemochromatosis monocytes and monocyte‐derived macrophages
Moura, Verheul, & Marx, J. J. M. (1998) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.1998.00263.x · Cited by 30
Hoffmann, A., Haschka, D., de Souza, L. V., Tymoszuk, P., Seifert, M., von Raffay, L., Hilbe, R., Petzer, V., Moser, P. L., Nairz, M., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103568 · Cited by 31
“[57] Bullen JJ, Spalding PB, Ward CG, Gutteridge JM.”
BackgroundBlunted hepcidin response to inflammation in the absence of Hfe and transferrin receptor 2
Wallace, D. F., McDonald, C. J., Ostini, L., & Subramaniam, V. N. (2011) · Blood · doi:10.1182/blood-2010-08-303859 · Cited by 29
Severe anaemia, iron deficiency, and susceptibility to invasive bacterial infections
Abuga, K. M., Nairz, M., MacLennan, C. A., & Atkinson, S. H. (2023) · Wellcome Open Research · doi:10.12688/wellcomeopenres.18829.1 · Cited by 31
Kim, G., Lee, S., Luong, T. T., Nguyen, C. T., Park, S., Pyo, S.-N., & Rhee, D. (2017) · Archives of Pharmacal Research · doi:10.1007/s12272-017-0931-0 · Cited by 27
“Furthermore, one of the vital nutrients, iron, is required for bacterial growth and replication (Skaar 2010); in the blood of patients with hemochromatosis, Vibrio vulnificus grows rapidly with iron overload (Bullen et al. 1991), suggesting that an excess of a nutrient can increase the virulence of pathogens.”
BackgroundLiu, M., & Crosa, J. H. (2012) · MicrobiologyOpen · doi:10.1002/mbo3.48 · Cited by 27
“In most of these patients, iron is present at higher than physiological level (Bullen et al. 1991; Hor et al. 1999).”
BackgroundFatalVibrio parahemolyticus septicemia in a patient with cirrhosis
Hally, R. J., Rubin, R. A., Fraimow, H. S., et al. (1995) · Digestive Diseases and Sciences · doi:10.1007/bf02065534 · Cited by 27
Vibrio vulnificus Damages Macrophages during the Early Phase of Infection
Tsuchiya, T., Mitsuo, E., Hayashi, N., Hikita, Y., Nakao, H., Yamamoto, S., Miyamoto, K., & Tsujibo, H. (2007) · Infection and Immunity · doi:10.1128/iai.00481-07 · Cited by 27
“vulnificus is associated with predisposing conditions such as hepatitis, cirrhosis, diabetes, hemochromatosis, and immune compromise (1, 2, 15, 22).”
BackgroundHemochromatosis and Iron Overload: From Bench to Clinic
Barton, J. C. (2013) · The American Journal of the Medical Sciences · doi:10.1097/maj.0000000000000192 · Cited by 28
Kim, C., Chung, Y., & Shin, S. (2009) · The Journal of Infectious Diseases · doi:10.1086/600869 · Cited by 25
Miller, H. K., Schwiesow, L., Au‐Yeung, W., & Auerbuch, V. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00069 · Cited by 25
“…of HH hosts is due to increased virulence of the pathogen, enhanced bacterial fitness due to increased iron availability, or a combination of these factors (Sinkovics et al., 1980; Christopher, 1985; Abbott et al., 1986; Bullen et al., 1991; Mennecier et al., 2001a; Harris and Paraskevakis, 2012).”
BackgroundNovel host‐specific iron acquisition system in the zoonotic pathogen V ibrio vulnificus
Pajuelo, D., Lee, C., Roig, F. J., Hor, L., & Amaro, C. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.12782 · Cited by 24
Excess dietary iron is the root cause for increase in childhood Autism and allergies
Padhye, U. (2003) · Medical Hypotheses · doi:10.1016/s0306-9877(03)00126-9 · Cited by 24
Phospholipase A as a potent virulence factor of Vibrio vulnificus
Koo, B.-S., Lee, J., Kim, S.-C., et al. (2007) · International Journal of Molecular Medicine · doi:10.3892/ijmm.20.6.913 · Cited by 23
Septic shock due toVibrio vulnificus serogroup 04 wound infection acquired from the Baltic Sea
Hoyer, J. D., Engelmann, E., Liehr, R., et al. (1995) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/bf01691388 · Cited by 23
Tajiri, T., Tate, G., Masunaga, A., et al. (2012) · Journal of Infection and Chemotherapy · doi:10.1007/s10156-012-0384-9 · Cited by 22
“Patients with liver cirrhosis show decreased neutrophil activity as a result of iron overloading [40, 41].”
BackgroundShin, N.-R., Lee, D., Shin, S. J., et al. (2004) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2004.03.001 · Cited by 22
“However, it increases to about 70% in the case of people who have chronic diseases that affect either the liver function or the immune system, such as cirrhosis, alcoholism, hepatitis and immunosuppressive disease [2–5].”
BackgroundProkocimer, M., & Potasman, I. (2008) · Postgraduate Medical Journal · doi:10.1136/pgmj.2008.069609 · Cited by 20
Shin, N.-R., Lee, D. Y., & Yoo, H. S. (2007) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2007.00236.x · Cited by 20
“All rights reserved Downloaded from https://academic.oup.com/femspd/article-abstract/50/1/94/505859 by guest on 29 July 2018 cirrhosis, or alcoholism (Nealson & Hastings, 1979; Brent et al., 1991; Bullen et al., 1991; Chan et al., 1994).”
MethodCytotoxic mechanism of vibrio vulnificus cytolysin in CPAE cells
Rho, H., Choi, M.-J., Lee, J.-N., et al. (2002) · Life Sciences · doi:10.1016/s0024-3205(02)01480-7 · Cited by 20
Lee, C., Amaro, C., Sanjuán, E., et al. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.9.5593-5597.2005 · Cited by 20
“In humans, this organism may cause serious wound infections and septicemia with a high mortality rate, particularly in people with underlying conditions such as alcoholism hemochromatosis, and liver cirrhosis (12, 25).”
Metadata
- Authors
- Bullen, J. J.
- Affiliations
- University of Miami (US)
- Corresponding author
- Bullen, John J.
- Venue
- Archives of Internal Medicine
- Publisher
- American Medical Association (AMA)
- Published
- 1991-08-01
- Volume
- 151
- Issue
- 8
- Pages
- 1606
- ISSN
- 0003-9926 (ISSN-L)
- OpenAlex
- W1998616787
- Semantic Scholar
- ad2466c97dc95a56572caa2fd685aab9f096f40f
- Cited by
- 190
- References
- 19
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 7 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 5 · 2017: 8 · 2016: 2 · 2015: 10 · 2014: 9 · 2013: 12 · 2012: 8
- FWCI
- 2.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Archives of Internal Medicine (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Vibrio bacteria research studies
- Health Sciences › Medicine › Microbiology (medical) › Infections and bacterial resistance
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Keywords
- hemochromatosis, Vibrio vulnificus, septicemia, iron overload, transferrin saturation, hematin, iron availability, chronic iron overload
- MeSH terms
- Female, Hemochromatosis, Hemoglobins, Humans, Iron, Male, Molecular Weight, Reference Values, Transferrin, Vibrio Infections, Sepsis, In Vitro Techniques
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