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December 1995, Vol 130, No. 12 >
ARTICLE | December 1995

Immunosuppression Augments Growth of Graft-Adherent Staphylococcus epidermidis FREE

Thomas M. Bergamini, MD; Roberto A. Corpus, Jr; Terry M. McCurry; James C. Peyton, MS; Kenneth R. Brittian; William G. Cheadle, MD
Arch Surg. 1995;130(12):1345-1350. doi:10.1001/archsurg.1995.01430120099015
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Objective:  To determine if systemic suppression of host defenses during graft implantation alters the initial adherence and subsequent growth of Staphylococcus epidermidis on vascular prostheses.

Design:  Dacron grafts 1 cm2 were implanted in the back subcutaneous tissue of Swiss-Webster mice (n=247), followed by topical inoculation with 2×107, 2×105, 2×103, or 2×101 colony-forming units of S epidermidis. Half of the mice were immunosuppressed with cyclophosphamide (150 mg/kg intraperitoneally), to achieve a consistent, significant decrease in the white blood cell count and major histocompatibility complex class II (Ia) expression. Control mice received an equal volume of saline solution. Graft bacterial biofilm concentrations were determined at 1 day for adherence and within 2 weeks for bacterial growth, by using sonication and quantitative agar culture.

Results:  Immunosuppression did not significantly alter the initial adherence of bacteria to vascular grafts. Immunosuppressed animals that were inoculated with 2×107 and 2×105 colony-forming units of S epidermidis had significantly higher bacterial biofilm concentrations as compared with those in control animals. Graft infection persisted at 14 days in all animals, with and without immunosuppression.

Conclusions:  Suppression of immune function during graft implantation augmented growth of adherent bacteria. The effect of short-term perioperative immunosuppression on late-appearing S epidermidis graft infection needs further study.(Arch Surg. 1995;130:1345-1350)

REFERENCES

1 +
Gristina AG, Costerton JW.  Bacteria-laden biofilms: a hazard to orthopedic prostheses . Infect Surg . 1984;;3:655-662.
2 +
Ludlam HA, Noble WC, Marples RR, Bayston R, Phillips I.  The epidemiology of peritonitis caused by coagulase-negative staphylococci in continuous ambulatory peritoneal dialysis . J Med Microbiol . 1989;;30:167-174.
3 +
Younger JJ, Christensen GD, Bartley DL, Simmons JCH, Barrett FF.  Coagulase-negative staphylococci isolated from cerebrospinal fluid shunts: importance of slime production, species identification, and shunt removal to clinical outcome . J Infect Dis . 1987;:156:548-554.
4 +
Bergamini TM.  Vascular prostheses infection caused by bacterial biofilms . Semin Vasc Surg . 1990;;3:101-109.
5 +
Passerini L, Lam K, Costerton JW, King G.  Biofilms on indwelling vascular catheters . Crit Care Med . 1992;;20:665-673.
6 +
Towne JB, Seabrook GR, Bandyk D, Freischlag JA, Edmiston CE.  In situ replacement of arterial prosthesis infected by bacterial biofilms: long-term follow-up . J Vasc Surg . 1994;;19:226-235.
7 +
Gemmell CG.  Pathogenicity of coagulase-negative staphylococci with respect to the nature of the host defense . Zentralbl Bakt Hyg . 1987;;A-266:52-59.
8 +
Wade JC, Schimpff SC, Newman KA, Wiernik PH.  Staphylococcus epidermidis: an increasing cause of infection in patients with granulocytopenia . Ann Intern Med . 1982;;97:503-508.
9 +
Forse RA, Dixon C, Bernard K, Martinez L, McLean PH, Meakins JL.  Staphylococcus epidermidis: an important pathogen . Surgery . 1979;;86:507-514.
10 +
Lamperi S, Carozzi S.  Immunologic defenses in CAPD . Curr Concepts CAPD Blood Purif . 1989;;7:126-143.
11 +
Meakins JL.  Surgeons, surgery, and immunomodulation . Arch Surg . 1991;; 126:494-498.
12 +
Keane RM, Munster AM, Birmingham W, Winchurch RA, Gadacz TR, Ernst CB.  Suppression of lymphocyte function after aortic reconstruction . Arch Surg . 1982;;117:1133-1135.
13 +
Roumen RMH, Hendriks T, van der Ven-Jongekrijg J, et al.  Cytokine patterns in patients after major vascular surgery, hemorrhagic shock, and severe blunt trauma . Ann Surg . 1993;;218:769-776.
14 +
Livingston DH, Appel SH, Wellhausen SR, Sonnenfeld G, Polk HC.  Depressed interferon-gamma production and monocyte HLA-DR expression after severe injury . Arch Surg . 1988;:123:1309.
15 +
Chaudry IH, Ayala A, Ertel W, Stephen RN.  Hemorrhage and resuscitation: Immunological aspects . Am J Physiol . 1990;;259:R663.
16 +
Naziri W, Pietsch JD, Appel SH, Cheadle WG, Bergamini TM, Polk HC Jr.  Hemorrhagic shock-induced alterations in circulating and bronchoalveolar macro-phage phage nitric oxide production . J Surg Res . 1995;;59:146-152.
17 +
Bergamini TM, Corpus RA Jr, Brittian KR, Peyton JC, Cheadle WG.  The natural history of bacterial biofilm graft infection . J Surg Res . 1994;;56:393-396.
18 +
Bergamini TM, Bandyk DF, Govostis D, Kaebnick HW, Towne JB.  Infection of vascular prostheses caused by bacterial biofilms . J Vasc Surg . 1988;;7:21-30.
19 +
Kaupp HA, Matulewicz TJ, Lattimer GL, Kremen JE, Celani VJ.  Graft infection or graft reaction? Arch Surg . 1979;;114:1419-1422.
20 +
Bamberger DM, Herndon BL.  Bactericidal capacity of neutrophils in rabbits with experimental acute and chronic abscesses . J Infect Dis . 1990;;162:186-192.
21 +
Ahn SS, Williams DE, Thye DA, Cheng KQ, Lee DA.  The isolation of a fibro-blast growth inhibitor associated with perigraft seroma . J Vasc Surg . 1994;; 20:202-208.
22 +
Modun B, Williams P, Pike WJ, et al.  Cell envelope proteins of Staphylococcus epidermidis grown in vivo in a peritoneal chamber implant . Infect Immun . 1992;; 60:2551-2553.
23 +
Gray ED, Peters G, Verstegen M, Regelmann WE.  Effect of extracellular slime substance from Staphylococcus epidermidis on the human cellular immune response . Lancet . 1984;;1:365-367.
24 +
Kaplan SS, Basford RE, Kormos RL, et al.  Biomaterial-associated impairment of local neutrophil function . ASAIO J . 1990;;36:M172-M175.
25 +
Noble MA, Grant SK, Hajen E.  Characterization of a neutrophil-inhibitory factor from clinically significant Staphylococcus epidermidis . J Infect Dis . 1990;;162: 909-913.
26 +
Garrison JR, Brittian KR, Lam TM, Peyton JC, Bergamini TM. MHC II: expression is decreased in Staphylococcus epidermidis graft infection. Presented at The Society of University Surgeons Thirty-seventh Annual University Surgical Residents' Conference; February 11, 1995; Denver, Colo.
27 +
Costerton JW, Geesey GG, Cheng K-J.  How bacteria stick . Sci Am . 1978;;238: 86-95.
28 +
Gristina AG, Costerton JW.  Bacterial adherence to biomaterials and tissue: the significance of its role in clinical sepsis . J Bone Joint Surg Am . 1985;;67:264-273.
29 +
Schmitt DD, Bandyk DF, Pequet AJ, Towne JB.  Bacterial adherence to vascular prostheses: a determinant of graft infectivity . J Vasc Surg . 1986;;3:732-740.
30 +
Levy MF, Schmitt DD, Edmiston CE, et al.  Sequential analysis of staphylococcal colonization of body surfaces of patients undergoing vascular surgery . J Clin Microbiol . 1990;;28:664-669.
31 +
Rosenman JE, Pearce WH, Kempczinski RF.  Bacterial adherence to vascular grafts after in vitro bacteremia . J Surg Res . 1985;;38:648-655.
32 +
Harris JM, Martin LF.  An in vitro study of the properties influencing Staphylococcus epidermidis adhesion to prosthetic vascular graft materials . Ann Surg . 1987;;206:612-620.
33 +
Deighton MA, Balkau B.  Adherence measured by microtiter assay as a virulence marker for Staphylococcus epidermidis infections . J Clin Microbiol . 1990;; 28:2442-2447.
34 +
Hawthorn L, Reid G.  The effect of protein and urine on uropathogen adhersion to polymer substrata . J Biomed Mater Res . 1990;;24:1325-1332.
35 +
Russell PB, Kline J, Yoder MC, Polin RA.  Staphylococcal adherence to polyvinyl chloride and heparin-bonded polyurethane catheters is species dependent and enhanced by fibronectin . J Clin Microbiol . 1987;;25:1083-1087.
36 +
Vaudaux P, Pittet D, Haeberli A, et al.  Host factors selectively increase staphylococcal adherence on inserted catheters: a role for fibronectin and fibrinogen or fibrin . J Infect Dis . 1989;;160:865-875.
37 +
Cheung AL, Fischetti VA.  The role of fibrinogen in mediating staphylococcal adherence to fibers . J Surg Res . 1991;;50:150-155.
38 +
Schmitt DD, Bandyk DF, Pequet AJ, Malangoni MA, Towne JB.  Mucin production by Staphylococcus epidermidis . Arch Surg . 1986;;121:89-95.
39 +
Farber BF, Wolff AG.  The use of nonsteroidal antiinflammatory drugs to prevent adherence of Staphylococcus epidermidis to medical polymers . J Infect Dis . 1992;;166:861-865.
40 +
Kojima Y, Tojo M, Goldmann DA, Tosteson TD, Pier GB.  Antibody to the capsular polysaccharide/adhesin protects rabbits against catheter-related bacteremia due to coagulase-negative staphylococci . J Infect Dis . 1990;;162:435-441.

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1 +
Gristina AG, Costerton JW.  Bacteria-laden biofilms: a hazard to orthopedic prostheses . Infect Surg . 1984;;3:655-662.
2 +
Ludlam HA, Noble WC, Marples RR, Bayston R, Phillips I.  The epidemiology of peritonitis caused by coagulase-negative staphylococci in continuous ambulatory peritoneal dialysis . J Med Microbiol . 1989;;30:167-174.
3 +
Younger JJ, Christensen GD, Bartley DL, Simmons JCH, Barrett FF.  Coagulase-negative staphylococci isolated from cerebrospinal fluid shunts: importance of slime production, species identification, and shunt removal to clinical outcome . J Infect Dis . 1987;:156:548-554.
4 +
Bergamini TM.  Vascular prostheses infection caused by bacterial biofilms . Semin Vasc Surg . 1990;;3:101-109.
5 +
Passerini L, Lam K, Costerton JW, King G.  Biofilms on indwelling vascular catheters . Crit Care Med . 1992;;20:665-673.
6 +
Towne JB, Seabrook GR, Bandyk D, Freischlag JA, Edmiston CE.  In situ replacement of arterial prosthesis infected by bacterial biofilms: long-term follow-up . J Vasc Surg . 1994;;19:226-235.
7 +
Gemmell CG.  Pathogenicity of coagulase-negative staphylococci with respect to the nature of the host defense . Zentralbl Bakt Hyg . 1987;;A-266:52-59.
8 +
Wade JC, Schimpff SC, Newman KA, Wiernik PH.  Staphylococcus epidermidis: an increasing cause of infection in patients with granulocytopenia . Ann Intern Med . 1982;;97:503-508.
9 +
Forse RA, Dixon C, Bernard K, Martinez L, McLean PH, Meakins JL.  Staphylococcus epidermidis: an important pathogen . Surgery . 1979;;86:507-514.
10 +
Lamperi S, Carozzi S.  Immunologic defenses in CAPD . Curr Concepts CAPD Blood Purif . 1989;;7:126-143.
11 +
Meakins JL.  Surgeons, surgery, and immunomodulation . Arch Surg . 1991;; 126:494-498.
12 +
Keane RM, Munster AM, Birmingham W, Winchurch RA, Gadacz TR, Ernst CB.  Suppression of lymphocyte function after aortic reconstruction . Arch Surg . 1982;;117:1133-1135.
13 +
Roumen RMH, Hendriks T, van der Ven-Jongekrijg J, et al.  Cytokine patterns in patients after major vascular surgery, hemorrhagic shock, and severe blunt trauma . Ann Surg . 1993;;218:769-776.
14 +
Livingston DH, Appel SH, Wellhausen SR, Sonnenfeld G, Polk HC.  Depressed interferon-gamma production and monocyte HLA-DR expression after severe injury . Arch Surg . 1988;:123:1309.
15 +
Chaudry IH, Ayala A, Ertel W, Stephen RN.  Hemorrhage and resuscitation: Immunological aspects . Am J Physiol . 1990;;259:R663.
16 +
Naziri W, Pietsch JD, Appel SH, Cheadle WG, Bergamini TM, Polk HC Jr.  Hemorrhagic shock-induced alterations in circulating and bronchoalveolar macro-phage phage nitric oxide production . J Surg Res . 1995;;59:146-152.
17 +
Bergamini TM, Corpus RA Jr, Brittian KR, Peyton JC, Cheadle WG.  The natural history of bacterial biofilm graft infection . J Surg Res . 1994;;56:393-396.
18 +
Bergamini TM, Bandyk DF, Govostis D, Kaebnick HW, Towne JB.  Infection of vascular prostheses caused by bacterial biofilms . J Vasc Surg . 1988;;7:21-30.
19 +
Kaupp HA, Matulewicz TJ, Lattimer GL, Kremen JE, Celani VJ.  Graft infection or graft reaction? Arch Surg . 1979;;114:1419-1422.
20 +
Bamberger DM, Herndon BL.  Bactericidal capacity of neutrophils in rabbits with experimental acute and chronic abscesses . J Infect Dis . 1990;;162:186-192.
21 +
Ahn SS, Williams DE, Thye DA, Cheng KQ, Lee DA.  The isolation of a fibro-blast growth inhibitor associated with perigraft seroma . J Vasc Surg . 1994;; 20:202-208.
22 +
Modun B, Williams P, Pike WJ, et al.  Cell envelope proteins of Staphylococcus epidermidis grown in vivo in a peritoneal chamber implant . Infect Immun . 1992;; 60:2551-2553.
23 +
Gray ED, Peters G, Verstegen M, Regelmann WE.  Effect of extracellular slime substance from Staphylococcus epidermidis on the human cellular immune response . Lancet . 1984;;1:365-367.
24 +
Kaplan SS, Basford RE, Kormos RL, et al.  Biomaterial-associated impairment of local neutrophil function . ASAIO J . 1990;;36:M172-M175.
25 +
Noble MA, Grant SK, Hajen E.  Characterization of a neutrophil-inhibitory factor from clinically significant Staphylococcus epidermidis . J Infect Dis . 1990;;162: 909-913.
26 +
Garrison JR, Brittian KR, Lam TM, Peyton JC, Bergamini TM. MHC II: expression is decreased in Staphylococcus epidermidis graft infection. Presented at The Society of University Surgeons Thirty-seventh Annual University Surgical Residents' Conference; February 11, 1995; Denver, Colo.
27 +
Costerton JW, Geesey GG, Cheng K-J.  How bacteria stick . Sci Am . 1978;;238: 86-95.
28 +
Gristina AG, Costerton JW.  Bacterial adherence to biomaterials and tissue: the significance of its role in clinical sepsis . J Bone Joint Surg Am . 1985;;67:264-273.
29 +
Schmitt DD, Bandyk DF, Pequet AJ, Towne JB.  Bacterial adherence to vascular prostheses: a determinant of graft infectivity . J Vasc Surg . 1986;;3:732-740.
30 +
Levy MF, Schmitt DD, Edmiston CE, et al.  Sequential analysis of staphylococcal colonization of body surfaces of patients undergoing vascular surgery . J Clin Microbiol . 1990;;28:664-669.
31 +
Rosenman JE, Pearce WH, Kempczinski RF.  Bacterial adherence to vascular grafts after in vitro bacteremia . J Surg Res . 1985;;38:648-655.
32 +
Harris JM, Martin LF.  An in vitro study of the properties influencing Staphylococcus epidermidis adhesion to prosthetic vascular graft materials . Ann Surg . 1987;;206:612-620.
33 +
Deighton MA, Balkau B.  Adherence measured by microtiter assay as a virulence marker for Staphylococcus epidermidis infections . J Clin Microbiol . 1990;; 28:2442-2447.
34 +
Hawthorn L, Reid G.  The effect of protein and urine on uropathogen adhersion to polymer substrata . J Biomed Mater Res . 1990;;24:1325-1332.
35 +
Russell PB, Kline J, Yoder MC, Polin RA.  Staphylococcal adherence to polyvinyl chloride and heparin-bonded polyurethane catheters is species dependent and enhanced by fibronectin . J Clin Microbiol . 1987;;25:1083-1087.
36 +
Vaudaux P, Pittet D, Haeberli A, et al.  Host factors selectively increase staphylococcal adherence on inserted catheters: a role for fibronectin and fibrinogen or fibrin . J Infect Dis . 1989;;160:865-875.
37 +
Cheung AL, Fischetti VA.  The role of fibrinogen in mediating staphylococcal adherence to fibers . J Surg Res . 1991;;50:150-155.
38 +
Schmitt DD, Bandyk DF, Pequet AJ, Malangoni MA, Towne JB.  Mucin production by Staphylococcus epidermidis . Arch Surg . 1986;;121:89-95.
39 +
Farber BF, Wolff AG.  The use of nonsteroidal antiinflammatory drugs to prevent adherence of Staphylococcus epidermidis to medical polymers . J Infect Dis . 1992;;166:861-865.
40 +
Kojima Y, Tojo M, Goldmann DA, Tosteson TD, Pier GB.  Antibody to the capsular polysaccharide/adhesin protects rabbits against catheter-related bacteremia due to coagulase-negative staphylococci . J Infect Dis . 1990;;162:435-441.

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