1. bookVolume 57 (2018): Issue 2 (January 2018)
Journal Details
License
Format
Journal
eISSN
2545-3149
First Published
01 Mar 1961
Publication timeframe
4 times per year
Languages
English, Polish
access type Open Access

THE ROLE OF STAPHYLOCOCCUS AUREUSIN THE CLINICAL DIAGNOSIS OF DIABETIC PATIENTS

Published Online: 20 May 2019
Volume & Issue: Volume 57 (2018) - Issue 2 (January 2018)
Page range: 166 - 178
Received: 01 Sep 2017
Accepted: 01 Feb 2018
Journal Details
License
Format
Journal
eISSN
2545-3149
First Published
01 Mar 1961
Publication timeframe
4 times per year
Languages
English, Polish
Abstract

Discovering interactions between the etiology of the infection and diabetic patients’ immune system activity may be essential for the relevant clinical diagnosis. The dynamics of colonization of the nasal vestibule by Staphylococcus aureus and the development of the prevention strategies against infection are different for various populations. Moreover, the colonization of the nasal vestibule might involve both molecular and epidemiological ctorsfa. Researchers have reported that the identification of methicillin-resistant strains S. aureus(MRSA) with similar molecular characteristics allows to assess the ability of the microorganism to spread and the risk of infection in diabetic patients. Knowledge of these characteristics allows to take precautions in patients exposed to S. aureus. S. aureus is an ethiological factors of many severe diseases both in people with weakened immune system and in healthy individuals. Usually, excess weight and obesity contribute to the incidence of diabetes mellitus type 2 (DM2). However, the colonization by S. aureus is a probable risk factor for infection. Among S. aureus virulence factors, superantigens (SAgs) are essential for pathogenicity. The long-term effect of the superantigen toxic shock syndrome toxin-1 (TSST-1) might be glucose intolerance. This toxin also induces systemic inflammation as a result of the increased exotoxin concentration in blood, and, therefore, may be the causative factor of diabetes. Chronic exposure to staphylococcal superantigens may contribute to the development of diabetes, suggesting a need to conduct targeted therapies against S. aureus superantigens.

1. Introduction. 2. Risk factors for infection in patients with diabetes. 2.1. Immunodeficiency. 2.2. Obesity 2.3. Staphylococcal carriage. 3. Staphylococcal infections in patients with diabetes. 3.1. Staphylococcal superantigens. 3.2. Skin and soft tissue infections. 3.3.Diabetic foot syndrome. 3.4. Sepsis. 3.5. Infective endocarditis. 3.6. Acute purulent meningitis. 4. Vaccination. 5. Conclusions

Keywords

Słowa kluczowe

Alizargar J., Sharif M.R., Sharif A.: Risk factors of methicillin- resistant Staphylococcus aureus colonization in diabetic outpatients, a prospective cohort study. Int. J. Microbiol. Res.4, 147–151 (2013)Search in Google Scholar

Alonzo F., Torres V.J.: The bicomponent pore-forming leuco- cidins of Staphylococcus aureus. Microbiol. Mol. Biol. Rev. 78, 199–230 (2014)Search in Google Scholar

Badaru A., Pihoker C.: Type 2 diabetes in childhood: clinical characteristics and role of β-cell autoimmunity. Curr. Diab. Rep. 12, 75–81 (2012)10.1007/s11892-011-0247-2Search in Google Scholar

Burian M., Grumann D., Holtfreter S., Wolz C., Goerke C., Bröker B.M.: Expression of staphylococcal superantigens during nasal colonization is not sufficient to induce a systemic neutralizing antibody response in humans. Eur. J. Clin. Microbiol. Infect. Dis. 31, 251–256 (2012)Search in Google Scholar

Casqueiro J., Casqueiro J., Alves C.: Infections in patients with diabetes mellitus: A review of pathogenesis. Indian J. Endocrinol. Metab. 16, 27–36 (2012)Search in Google Scholar

Cervantes-García E., García-Gonzalez R., Reyes-Torres A., Resendiz-Albor A.A., Salazar-Schettino P.M.: Staphylococcus aureus small colony variants in diabetic foot infections. Diabet. Foot Ankle, 6, 26431 (2015)10.3402/dfa.v6.26431Search in Google Scholar

Dai X., Zhan J., Demmy T.A., Poordad F.B., Fauceglia P.L., Zhang H., Wu L.: Monocytes play different roles in stimulating T cells in obese diabetic individuals. Int. J. Immunopathol. Pharmacol.28, 374–383 (2015)10.1177/0394632015598848Search in Google Scholar

De Bus L., Coessens G., Boelens J., Claeys G., Decruyenaere J., Depuydt P.: Microbial etiology and antimicrobial resistance in healthcare-associated versus community-acquired and hospital-acquired bloodstream infection in a tertiary care hospital. Diagn. Microbiol. Infect. Dis. 77, 341–345 (2013)Search in Google Scholar

DeFuria J., Belkina A.C., Jagannathan-Bogdan M., Snyder- Cappione J., Carr J.D., Nersesova Y.R., Markham D., Stris- sel K.J., Watkins A.A., Zhu M., Allen J., Bouchard J., Toraldo G., Jasuja R., Obin M.S., McDonnell M.E., Apovian C., Denis G.V., Nikolajczyk B.S.: B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc. Natl. Acad. Sci. USA, 110, 5133–5138 (2013)10.1073/pnas.1215840110Search in Google Scholar

Dumont A.L., Nygaard T.K., Watkins R.L., Smith A., Kozhaya L., Kreiswirth B.N., Shopsin B., Unutmaz D., Voyich J.M., Torres V.J.: Characterization of a new cytotoxin that contributes to Staphylococcus aureus pathogenesis. Mol. Microbiol. 79, 814–825 (2011)Search in Google Scholar

Fast D.J., Schlievert P.M., Nelson R.D.: Nonpurulent response to toxic shock syndrome toxin 1-producing Staphylococcus aureus. Relationship to toxin-stimulated production of tumor Necrosis factor. J. Immunol. 140, 949–853 (1988)Search in Google Scholar

Fijałkowski K., Czernomysy-Furowicz G., Ferlas M.: Staphylococcus aureus versus the immune system. Post. Mikrobiol. 47, 497–501 (2008)Search in Google Scholar

Frasca D., Ferracci F., Diaz A., Romero M., Lechner S., Blomberg B.B.: Obesity decreases B cell responses in young and elderly individuals. Obesity (Silver Spring), 24 615–625 (2016)10.1002/oby.21383Search in Google Scholar

Fraser J.D., Proft T.: The bacterial superantigen and superantigen-like proteins. Immunol. Rev.225, 226–243 (2008)10.1111/j.1600-065X.2008.00681.xSearch in Google Scholar

Gillet Y., Etienne J. i wsp.: Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet, 359, 753–759 (2002)10.1016/S0140-6736(02)07877-7Search in Google Scholar

Gravet, A., Colin D.A., Keller D., Girardot R., Monteil H., Prévost G.: Characterization of a novel structural member, LukE-LukD, of the bi-component staphylococcal leucotoxins family. FEBS Lett. 436, 202–208 (1998)10.1016/S0014-5793(98)01130-2Search in Google Scholar

Guha M., Bai W., Nadler J.L., Natarajan R.: Molecular mechanisms of tumor necrosis factor alpha gene expression in monocytic cells via hyperglycemia-induced oxidant stress-dependent and -independent pathways. J. Biol. Chem. 275, 17728–17739 (2000)Search in Google Scholar

Hernandez C., Cobos-Trigueros N., Feher C., Morata L., De La Calle C., Marco F., Almela M., Soriano A., Mensa J., Del Rio A., Martinez J.A.: Community-onset bacteraemia of unknown origin: clinical characteristics, epidemiology and outcome. Eur. J. Clin. Microbiol. Infect. Dis. 33, 1973–1980 (2014)Search in Google Scholar

Holtfreter S., Bauer K., Thomas D., Feig C., Lorenz V., Roschack K., Friebe E., Selleng K., Lövenich S., Greve T., Greinacher A., Panzig B., Engelmann S., Lina G., Bröker B.M.: egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect. Immun.72, 4061–4071 (2004)10.1128/IAI.72.7.4061-4071.200442745815213151Search in Google Scholar

Huseby M.J., Kruse A.C., Digre J., Kohler P.L., Vocke J.A., Mann E.E., Bayles K.W., Bohach G.A., Schlievert P.M., Ohlen- dorf D.H., Earhart C.A.: Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. Proc. Natl. Acad. Sci. USA, 107, 14407–14412 (2010)10.1073/pnas.0911032107292255420660751Search in Google Scholar

Klein E., Smith D.L., Laxminarayan R.: Hospitalizations and deaths caused by methicillin- resistant Staphylococcus aureus, United States, 1999–2005. Emerg. Infect. Dis. 13, (2007)Search in Google Scholar

Klekotka R.B., Mizgała E., Król W.: The etiology of lower respiratory tract infections in people with diabetes. Pneumonol. Alergol. Pol. 83, 401–408 (2015)Search in Google Scholar

Kluytmans J., van Belkum A., Verbrugh H.: Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10, 505–520 (1997)10.1128/CMR.10.3.505Search in Google Scholar

Kulhankova K., King J., Salgado-Pabón W.: Staphylococcal toxic shock syndrome: superantigen-mediated enhancement of endotoxin shock and adaptive immune suppression. Immunol. Res. 59, 182–187 (2014)10.1007/s12026-014-8538-8Search in Google Scholar

Kübler A., Jaeschke R., Jankowski M.: Sepsis and septic shock. In Szczeklik A. (ed), Internal Diseases. The state of knowledge on year 2010. Practical Medicine, Kraków, s. 2200–2205 (2010)Search in Google Scholar

Laupland K.B., Gregson D.B., Zygun D.A., Doig C.J., Mortis G., Church D.L.: Severe bloodstream infections: a population-based assessment. Crit. Care Med. 32, 992–997 (2004)10.1097/01.CCM.0000119424.31648.1ESearch in Google Scholar

Lee P.K., Deringer J.R., Kreiswirth B.N., Novick R.P., Schlie- vert P.M.: Fluid replacement protection of rabbits challenged subcutaneous with toxic shock syndrome toxins. Infect. Immun. 59, 879–884 (1991)Search in Google Scholar

Lipsky B.A., Pecoraro R.E., Chen M.S., Koepsell T.D.: Factors affecting staphylococcal colonization among NIDDM outpatients. Diabetes Care, 10, 483–486 (1987)10.2337/diacare.10.4.483Search in Google Scholar

Lipsky B.A., Tabak Y.P., Johannes R.S., Vo L., Hyde L., Weigelt J.A.: Skin and soft tissue infections in hospitalized patients with diabetes: Culture isolates and risk factors associated with mortality, length of stay and cost. Diabetologia, 53, 914–923 (2010)10.1007/s00125-010-1672-5Search in Google Scholar

Lydyard P.M., Whelan A., Fanger M.W.: Short lectures. Immunology, Scientific Publishing PWN SA, Warszawa, s. 97–103 (2008)Search in Google Scholar

Małecki R., Rosiński K., Adamiec R.: Etiological factors of infections in diabetic foot syndrome – attempt to define optimal empirical therapy. Adv. Clin. Exp. Med. 23, 39–48 (2014)Search in Google Scholar

McKane C.K., Marmarelis M., Mendu M.L., Moromizato T., Gibbons F.K., Christopher K.B.: Diabetes mellitus and community-acquired bloodstream infections in the critically ill. J. Crit. Care.29, 70–76 (2014)10.1016/j.jcrc.2013.08.019Search in Google Scholar

Miro J.M., Fowler V.G. i wsp.: Staphylococcus aureus native valve infective endocarditis: report of 566 episodes from the International Collaboration on Endocarditis Merged Database. Clin. Infect. Dis. 41, 507–514 (2005)Search in Google Scholar

Mueller E.A., Merriman J.A., Schlievert P.M.: Toxic Shock Syndrome Toxin-1, Not Alpha Toxin, Mediated Bundaberg Fatalities. Microbiology, 161, 2361–2368 (2015)10.1099/mic.0.000196Search in Google Scholar

Muñoz P., Hortal J., Giannella M., Barrio J.M., Rodríguez- -Créixems M., Pérez M.J., Rincón C., Bouza E.: Nasal carriage of S. aureus increases the risk of surgical site infection after major heart surgery. J. Hosp. Infect. 68, 25–31 (2008)Search in Google Scholar

Naber C.K.: Staphylococcus aureus Bacteremia: Epidemiology, pathophysiology, and management strategies. Clin. Infect. Dis. 48, 231–237 (2009)Search in Google Scholar

Nada H.A., Gomaab N.I.M., Elakhrasa A., Wasfya R., Bakera A.: Skin colonization by superantigen-producing Staphylococcus aureus in Egyptian patients with atopic dermatitis and its relation to disease severity and serum interleukin-4 level. Int. J. Infect. Dis. 16, 29–33 (2012)Search in Google Scholar

Nienaber J.J., Sharma Kuinkel B.K., Clarke-Pearson M., Lamlert- thon S., Park L., Rude T.H., Barriere S., Woods C.W., Chu V.H., Marín M., Bukovski S., Garcia P., Corey G.R., Korman T., Doco- Lecompte T., Murdoch D.R., Reller L.B, Fowler V.G.: Methicillin-susceptible Staphylococcus aureus endocarditis isolates are associated with clonal complex 30 genotype and a distinct repertoire of enterotoxins and adhesins. J. Infect. Dis. 204, 704–713 (2011)Search in Google Scholar

Olokoba A.B., Obateru O.A., Olokoba L.B.: Type 2 diabetes mellitus: a review of current trends. Oman Med. J. 27, 269–273 (2012)Search in Google Scholar

Panton P.N., Valentine F.C.O.: Staphylococcal toxin. Lancet, 219, 506–508 (1932)10.1016/S0140-6736(01)24468-7Search in Google Scholar

Petrovici C.G., Dorobăt C., Bejan C., Juganariu G., Simiraş E., Filip O., Luca V., Miftode E.: Epidemiology and clinical features in diabetic patients with invasive infections treated at the Clinical Hospital of Infectious Diseases of laşi, Romania, between 2008–2010. Rev. Med. Chir. Soc. Med. Nat. Iasi.115, 1035–1041 (2011)Search in Google Scholar

Petrovici C.G., Leca D., Teodor A., Dorneanu O., Juganariu G., Dorobăt C., Egidia M.: Bacterial meningitis during sepsis in diabetic patient. Rev. Med. Chir. Soc. Med. Nat. Iasi.117, 901–907 (2013)Search in Google Scholar

Piya M.K., McTernan P.G., Kumar S.: Adipokine inflammation and insulin resistance: the role of glucose, lipids and endotoxin. J. Endocrinol. 216, T1-T15 (2013)10.1530/JOE-12-049823160966Search in Google Scholar

Poindexter N.J., Schlievert P.M.: Suppression of immunoglobu- lin-secreting cells from human peripheral blood by toxic-shocksyndrome toxin-1. J. Infect. Dis.153, 772–779 (1986)10.1093/infdis/153.4.7723512737Search in Google Scholar

Pragman A.A., Schlievert P.M.: Virulence regulation in Staphylococcus aureus: the need for in vivo analysis of virulence factor regulation. FEMS Immunol. Med. Microbiol. 42, 147–154 (2004)Search in Google Scholar

Price C.L., Al Hassi H.O., English N.R., Blakemore A.I., Stagg A.J., Knight S.C.: Methylglyoxal modulates immune responses: relevance to diabetes. J. Cell. Mol. Med. 14, 1806– 1815 (2010)Search in Google Scholar

Przyjałkowski W.: Central nervous system infections. In Szcze- klik A. (ed), Internal Diseases. The state of knowledge on year 2010, Practical Medicine, Kraków, s. 2149–2171 (2010)Search in Google Scholar

Rodríguez E.A., Correa M.M., Ospina S., Atehortúa S.L., Jimé- nez J.N.: Differences in epidemiological and molecular characteristics of nasal colonization with Staphylococcus aureus(MSSA-MRSA) in children from a university hospital and day care centers. Plos One, 9, e101417 (2014)10.1371/journal.pone.0101417407929824987854Search in Google Scholar

Roliński J., Sacha T., Immunosuppression. In Szczeklik A. (ed), Internal Diseases. The state of knowledge on year 2010, Practical Medicine, Kraków, s. 1599–1608 (2010)Search in Google Scholar

Salgado-Pabón W., Breshears L., Spaulding A.R., Merriman J.A., Stach C.S., Horswill A.R., Peterson M.L., Schlievert P.M.: Superantigens are critical for Staphylococcus aureus Infective endocarditis, sepsis, and acute kidney injury. M. bio.4, 00494–00513 (2013)10.1128/mBio.00494-13374758623963178Search in Google Scholar

Salgado-Pabón W., Schlievert P.M.: Models matter: the search for an effective Staphylococcus aureus vaccine. Nat. Rev. Microbiol. 12, 585–591 (2014)10.1038/nrmicro330824998740Search in Google Scholar

Shah B.R., Huh J.E.: Quantifying the risk of infectious diseases for people with diabetes. Diabetes Care, 26, 510–513 (2003)10.2337/diacare.26.2.51012547890Search in Google Scholar

Shallcross L.J., Fragaszy E., Johnson A.M., Hayward AC.: The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis. Lancet Infect. Dis. 13, 43–54 (2013)Search in Google Scholar

Shambat M., Haggar S., Vandenesch A., Lina F., van Wamel G., Arakere W.J., Swensson G., Norrby-Teglund M.A.: Levels of alpha-toxin correlate with distinct phenotypic response profiles of blood mononuclear cells and with agr background of community-associated Staphylococcus aureus isolates. Plos One, 9, e106107 (2014)10.1371/journal.pone.0106107414839825166615Search in Google Scholar

Sieradzki J.: Diabetes mellitus and metabolic syndrome. In Szczeklik A. (ed), Internal Diseases. The state of knowledge on year 2010, Practical Medicine, Kraków, , s. 1243–1284 (2010)Search in Google Scholar

Sollid J.U., Furberg A.S., Hanssen A.M., Johannessen M.: Staphylococcus aureus: determinants of human carriage. Infect. Genet. Evol. 21, 531–41 (2014)Search in Google Scholar

Spaan A.N., Schiepers A., de Haas C.J., van Hooijdonk D.D., Badiou C., Contamin H., Vandenesch F., Lina G., Gerard NP., Gerard C., van Kessel K.P., Henry T., van Strijp J.A.: Differential Interaction of the Staphylococcal Toxins Panton-Valentine Leukocidin and γ-Hemolysin CB with Human C5a Receptors. J. Immunol. 195, 1034–1043 (2015).10.4049/jimmunol.1500604450685326091719Search in Google Scholar

Spaulding A.R., Salgado-Pabón W., Kohler P.L., Horswill A.R., Leung D.Y., Schlievert P.M.: Staphylococcal and streptococcal superantigen exotoxins. Clin. Microbiol. Rev. 26, 422–447 (2013)Search in Google Scholar

Spaulding A.R., Satterwhite E.A., Lin Y.C., Chuang-Smith O.N., Frank K.L., Merriman J.A., Schaefers M.M., Yarwood J.M., Peterson M.L., Schlievert P.M.: Comparison of Staphylococcus aureus strains for ability to cause infective endocarditis and lethal sepsis in rabbits. Front. Cell. Infect. Microbiol.2, 18 (2012)10.3389/fcimb.2012.00018341757422919610Search in Google Scholar

Stoeckle M., Kaech C., Trampuz A., Zimmerli W.: The role of diabetes mellitus in patients with bloodstream infections. Swiss Med. Wkly. 138, 512–529 (2008)Search in Google Scholar

van Belkum A., Verkaik N.J., de Vogel C.P., Boelens H.A., Verveer J., Nouwen J.L., Verbrugh H.A., Wertheim H.F.L.: Reclassification of Staphylococcus aureus nasal carriage types. J. Infect. Dis. 15, 199,1820–1826 (2009)Search in Google Scholar

Vandenesch F., Naimi T., Enright M.C., Lina G., Nimmo G.R., Heffernan H., Liassine N., Bes M., Greenland T., Reverdy M.E., Etienne J.: Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg. Infect. Dis. 9, 978–984 (2003)Search in Google Scholar

Voyich J.M., Braughton K.R., Sturdevant D.E., Whitney A.R., Saïd-Salim B., Porcella S.F., Long R.D., Dorward D.W., Gardner D.J., Kreiswirth B.N., Musser JM., DeLeo F.R.: Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175, 3907–3919 (2005)10.4049/jimmunol.175.6.390716148137Search in Google Scholar

Vu B.G., Gourronc F.A., Bernlohr D.A., Schlievert P.M., Klingel- hutz A.J.: Staphylococcal superantigens stimulate immortalized human adipocytes to produce chemokines. Plos One,8, e77988 (2013)10.1371/journal.pone.0077988381349524205055Search in Google Scholar

Vu B.G., Stach C.S., Kulhankova K., Salgado-Pabón W., Klingel- hutz A.J, Schlievert PM.: Chronic superantigen exposure induces systemic inflammation, elevated bloodstream endotoxin, and abnormal glucose tolerance in rabbits: possible role in diabetes. M. Bio. 24, e02554 (2015)10.1128/mBio.02554-14435800725714716Search in Google Scholar

Vu B.G., Stach C.S., Salgado-Pabón W., Diekema D.J., Gardner S.E., Schlievert P.M.: Superantigens of Staphylococcus aureusfrom patients with diabetic foot ulcers. J. Infect. Dis. 210, 1920– 1927 (2014)Search in Google Scholar

Wertheim H.F., Melles D.C., Vos M.C., van Leeuwen W., van Belkum A., Verbrugh H.A., Nouwen J.L.: The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 5, 751–762 (2005)Search in Google Scholar

Xiong Y.Q., Willard J., Yeaman M.R., Cheung A.L., Bayer A.S.: Regulation of Staphylococcus aureus alpha-toxin gene (hla) expression by agr, sarA, and sae in vitro and in experimental infective endocarditis. J. Infect. Dis.194, 1267–1275 (2006)10.1086/50821017041853Search in Google Scholar

Yazdanpanah L., Nasiri M., Adarvishi S.: Literature review on the management of diabetic foot ulcer. World J. Diabetes. 15, 37–53 (2015)Search in Google Scholar

Zhai X., Qian G., Wang Y., Chen X., Lu J., Zhang Y., Huang Q., Wang Q.: Elevated B Cell Activation is Associated with Type 2 Diabetes Development in Obese Subjects. Cell. Physiol. Biochem. 38, 1257–1266 (2016)Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo