Markers of bacterial translocation in end-stage liver disease

World Journal of Hepatology

Volumn 7, Issue 20, 2015, Pages 2264-2273

  Koutsounas, Ioannis ^a   Kaltsa, Garyfallia ^a   Siakavellas, Spyros I ^a   Bamias, Giorgos ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

Bacterial DNA; Bacterial translocation; Biomarkers; Calprotectin; Cirrhosis; End stage liver disease; Lipopolysaccharide binding protein; Lipopolysaccharides endotoxin; Procalcitonin; Soluble CD14

Indexed keywords

EID: 84943391398     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v7.i20.2264     Document Type: Review

References (99)

1. Arvaniti V, D'Amico G, Fede G, Manousou P, Tsochatzis E, Pleguezuelo M, Burroughs AK. Infections in patients with cirrhosis increase mortality four-fold and should be used in determining prognosis. Gastroenterology 2010; 139: 1246-1256, 1256.e1-5 [PMID:20558165 DOI:10.1053/j.gastro.2010.06.019]
2. Deschênes M, Villeneuve JP. Risk factors for the development of bacterial infections in hospitalized patients with cirrhosis. Am J Gastroenterol 1999; 94: 2193-2197 [PMID:10445549 DOI:10.1111/j.1572-0241.1999.01293.x]
3. Fernández J, Navasa M, Gómez J, Colmenero J, Vila J, Arroyo V, Rodés J. Bacterial infections in cirrhosis: epidemiological changes with invasive procedures and norfloxacin prophylaxis. Hepatology 2002; 35: 140-148 [PMID:11786970 DOI:10.1053/jhep.2002.30082]
4. Berg RD, Garlington AW. Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun 1979; 23: 403-411 [PMID:154474]
5. Bellot P, Francés R, Such J. Pathological bacterial translocation in cirrhosis: pathophysiology, diagnosis and clinical implications. Liver Int 2013; 33: 31-39 [PMID:23121656 DOI:10.1111/liv.12021]
6. Wiest R, Rath HC. Gastrointestinal disorders of the critically ill. Bacterial translocation in the gut. Best Pract Res Clin Gastroenterol 2003; 17: 397-425 [PMID:12763504 DOI:10.1016/S1521-6918(03)00024-6]
7. Gasbarrini A, Lauritano EC, Gabrielli M, Scarpellini E, Lupascu A, Ojetti V, Gasbarrini G. Small intestinal bacterial overgrowth: diagnosis and treatment. Dig Dis 2007; 25: 237-240 [PMID:17827947 DOI:10.1159/000103892]
8. Pérez-Paramo M, Muñoz J, Albillos A, Freile I, Portero F, Santos M, Ortiz-Berrocal J. Effect of propranolol on the factors promoting bacterial translocation in cirrhotic rats with ascites. Hepatology 2000; 31: 43-48 [PMID:10613726 DOI:10.1002/hep.510310109]
9. Yang CY, Chang CS, Chen GH. Small-intestinal bacterial overgrowth in patients with liver cirrhosis, diagnosed with glucose H2 or CH4 breath tests. Scand J Gastroenterol 1998; 33: 867-871 [PMID:9754736 DOI:10.1080/00365529850171549]
10. Chang CS, Chen GH, Lien HC, Yeh HZ. Small intestine dysmotility and bacterial overgrowth in cirrhotic patients with spontaneous bacterial peritonitis. Hepatology 1998; 28: 1187-1190 [PMID:9794900 DOI:10.1002/hep.510280504]
11. Such J, Guardiola JV, de Juan J, Casellas JA, Pascual S, Aparicio JR, Solá-Vera J, Pérez-Mateo M. Ultrastructural characteristics of distal duodenum mucosa in patients with cirrhosis. Eur J Gastroenterol Hepatol 2002; 14: 371-376 [PMID:11943948 DOI:10.1097/00042737-200204000-00006]
12. Bertók L. Bile acids in physico-chemical host defence. Pathophysiology 2004; 11: 139-145 [PMID:15561510 DOI:10.1016/j.pathophys.2004.09.002]
13. Pascual S, Such J, Esteban A, Zapater P, Casellas JA, Aparicio JR, Girona E, Gutiérrez A, Carnices F, Palazón JM, Sola-Vera J, PérezMateo M. Intestinal permeability is increased in patients with advanced cirrhosis. Hepatogastroenterology 2003; 50: 1482-1486 [PMID:14571769]
14. MacDonald TT, Pettersson S. Bacterial regulation of intestinal immune responses. Inflamm Bowel Dis 2000; 6: 116-122 [PMID:10833071 DOI:10.1097/00054725-200005000-00008]
15. Heel KA, McCauley RD, Papadimitriou JM, Hall JC. Review: Peyer's patches. J Gastroenterol Hepatol 1997; 12: 122-136 [PMID:9083913 DOI:10.1111/j.1440-1746.1997.tb00395.x]
16. Rajkovic IA, Williams R. Abnormalities of neutrophil phagocytosis, intracellular killing and metabolic activity in alcoholic cirrhosis and hepatitis. Hepatology 1989; 6: 252-262 [PMID:3007318 DOI:10.1002/hep.1840060217]
17. Bolognesi M, Merkel C, Bianco S, Angeli P, Sacerdoti D, Amodio P, Gatta A. Clinical significance of the evaluation of hepatic reticuloendothelial removal capacity in patients with cirrhosis. Hepatology 1994; 19: 628-634 [PMID:8119687 DOI:10.1002/hep.1840190313]
18. Panés J, Pérez-del-Pulgar S, Casadevall M, Salas A, Pizcueta P, Bosch J, Anderson DC, Granger DN, Piqué JM. Impaired mesenteric leukocyte recruitment in experimental portal hypertension in the rat. Hepatology 1999; 30: 445-453 [PMID:10421653 DOI:10.1002/hep.510300214]
19. Albillos A, de la Hera A, González M, Moya JL, Calleja JL, Monserrat J, Ruiz-del-Arbol L, Alvarez-Mon M. Increased lipopolysaccharide binding protein in cirrhotic patients with marked immune and hemodynamic derangement. Hepatology 2003; 37: 208-217 [PMID:12500206 DOI:10.1053/jhep.2003.50038]
20. Bellot P, García-Pagán JC, Francés R, Abraldes JG, Navasa M, Pérez-Mateo M, Such J, Bosch J. Bacterial DNA translocation is associated with systemic circulatory abnormalities and intrahepatic endothelial dysfunction in patients with cirrhosis. Hepatology 2010; 52: 2044-2052 [PMID:20979050 DOI:10.1002/hep.23918]
21. Shah N, Dhar D, El Zahraa Mohammed F, Habtesion A, Davies NA, Jover-Cobos M, Macnaughtan J, Sharma V, Olde Damink SW, Mookerjee RP, Jalan R. Prevention of acute kidney injury in a rodent model of cirrhosis following selective gut decontamination is associated with reduced renal TLR4 expression. J Hepatol 2012; 56: 1047-1053 [PMID:22266601 DOI:10.1016/j.jhep.2011.11.024]
22. Kalambokis GN, Mouzaki A, Rodi M, Pappas K, Fotopoulos A, Xourgia X, Tsianos EV. Rifaximin improves systemic hemodynamics and renal function in patients with alcohol-related cirrhosis and ascites. Clin Gastroenterol Hepatol 2012; 10: 815-818 [PMID:22391344 DOI:10.1016/j.cgh.2012.02.025]
23. Baveja R, Keller S, Yokoyama Y, Sonin N, Clemens MG, Zhang JX. LPS-induced imbalanced expression of hepatic vascular stress genes in cirrhosis: possible mechanism of increased susceptibility to endotoxemia. Shock 2002; 17: 316-321 [PMID:11954834 DOI:10.1097/00024382-200204000-00014]
24. Thalheimer U, Triantos CK, Samonakis DN, Patch D, Burroughs AK. Infection, coagulation, and variceal bleeding in cirrhosis. Gut 2005; 54: 556-563 [PMID:15753544 DOI:10.1136/gut.2004.048181]
25. Vaquero J, Polson J, Chung C, Helenowski I, Schiodt FV, Reisch J, Lee WM, Blei AT. Infection and the progression of hepatic encephalopathy in acute liver failure. Gastroenterology 2003; 125: 755-764 [PMID:12949721 DOI:10.1016/S0016-5085(03)01051-5]
26. Sidhu SS, Goyal O, Mishra BP, Sood A, Chhina RS, Soni RK. Rifaximin improves psychometric performance and health-related quality of life in patients with minimal hepatic encephalopathy (the RIME Trial). Am J Gastroenterol 2011; 106: 307-316 [PMID:21157444 DOI:10.1038/ajg.2010.455]
27. Cirera I, Bauer TM, Navasa M, Vila J, Grande L, Taurá P, Fuster J, García-Valdecasas JC, Lacy A, Suárez MJ, Rimola A, Rodés J. Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol 2001; 34: 32-37 [PMID:11211904 DOI:10.1016/S0168-8278(00)00013-1]
28. Such J, Francés R, Muñoz C, Zapater P, Casellas JA, Cifuentes A, Rodríguez-Valera F, Pascual S, Sola-Vera J, Carnicer F, Uceda F, Palazón JM, Pérez-Mateo M. Detection and identification of bacterial DNA in patients with cirrhosis and culture-negative, nonneutrocytic ascites. Hepatology 2002; 36: 135-141 [PMID:12085357 DOI:10.1053/jhep.2002.33715]
29. Guarner C, González-Navajas JM, Sánchez E, Soriando G, Francés R, Chiva M, Zapater P, Benlloch S, Muñoz C, Pascual S, Balanzó J, Pérez-Mateo M, Such J. The detection of bacterial DNA in blood of rats with CCl4-induced cirrhosis with ascites represents episodes of bacterial translocation. Hepatology 2006; 44: 633-639 [PMID:16941689 DOI:10.1002/hep.21286]
30. Francés R, Benlloch S, Zapater P, González JM, Lozano B, Muñoz C, Pascual S, Casellas JA, Uceda F, Palazón JM, Carnicer F, PérezMateo M, Such J. A sequential study of serum bacterial DNA in patients with advanced cirrhosis and ascites. Hepatology 2004; 39: 484-491 [PMID:14768002 DOI:10.1002/hep.20055]
31. Francés R, Muñoz C, Zapater P, Uceda F, Gascón I, Pascual S, Pérez-Mateo M, Such J. Bacterial DNA activates cell mediated immune response and nitric oxide overproduction in peritoneal macrophages from patients with cirrhosis and ascites. Gut 2004; 53: 860-864 [PMID:15138214 DOI:10.1136/gut.2003.027425]
32. El-Naggar MM, Khalil el-SA, El-Daker MA, Salama MF. Bacterial DNA and its consequences in patients with cirrhosis and culture-negative, non-neutrocytic ascites. J Med Microbiol 2008; 57: 1533-1538 [PMID:19018026 DOI:10.1099/jmm.0.2008/001867-0]
33. González-Navajas JM, Bellot P, Francés R, Zapater P, Muñoz C, García-Pagán JC, Pascual S, Pérez-Mateo M, Bosch J, Such J. Presence of bacterial-DNA in cirrhosis identifies a subgroup of patients with marked inflammatory response not related to endotoxin. J Hepatol 2008; 48: 61-67 [PMID:17998145 DOI:10.1016/j.jhep.2007.08.012]
34. Zapater P, Francés R, González-Navajas JM, de la Hoz MA, Moreu R, Pascual S, Monfort D, Montoliu S, Vila C, Escudero A, Torras X, Cirera I, Llanos L, Guarner-Argente C, Palazón JM, Carnicer F, Bellot P, Guarner C, Planas R, Solá R, Serra MA, Muñoz C, Pérez-Mateo M, Such J. Serum and ascitic fluid bacterial DNA: a new independent prognostic factor in noninfected patients with cirrhosis. Hepatology 2008; 48: 1924-1931 [PMID:19003911 DOI:10.1002/hep.22564]
35. Jun DW, Kim KT, Lee OY, Chae JD, Son BK, Kim SH, Jo YJ, Park YS. Association between small intestinal bacterial overgrowth and peripheral bacterial DNA in cirrhotic patients. Dig Dis Sci 2010; 55: 1465-1471 [PMID:19517230 DOI:10.1007/s10620-009-0870-9]
36. Fagan KJ, Rogers GB, Melino M, Arthur DM, Costello ME, Morrison M, Powell EE, Irvine KM. Ascites bacterial burden and immune cell profile are associated with poor clinical outcomes in the absence of overt infection. PLoS One 2015; 10: e0120642 [PMID:25781164 DOI:10.1371/journal.pone.0120642]
37. Francés R, Zapater P, González-Navajas JM, Muñoz C, Caño R, Moreu R, Pascual S, Bellot P, Pérez-Mateo M, Such J. Bacterial DNA in patients with cirrhosis and noninfected ascites mimics the soluble immune response established in patients with spontaneous bacterial peritonitis. Hepatology 2008; 47: 978-985 [PMID:18306221 DOI:10.1002/hep.22083]
38. Mostafa MS, El-Seidi EA, Kassem AM, Shemis MA, Saber M, Michael MN. Detection of ascitic fluid infections in patients with liver cirrhosis and ascites. Arab J Gastroenterol 2011; 12: 20-24 [PMID:21429450 DOI:10.1016/j.ajg.2011.01.004]
39. Rincón D, Vaquero J, Hernando A, Galindo E, Ripoll C, Puerto M, Salcedo M, Francés R, Matilla A, Catalina MV, Clemente G, Such J, Bañares R. Oral probiotic VSL#3 attenuates the circulatory disturbances of patients with cirrhosis and ascites. Liver Int 2014; 34: 1504-1512 [PMID:24661740 DOI:10.1111/liv.12539]
40. Sersté T, Bert F, Leflon-Guibout V, Chauvet C, Marcon E, Asselah T, Francoz C, Durand F, Lebrec D, Valla D, Moreau R, Nicolas-Chanoine MH. Detection of bacterial DNA in serum and ascitic fluid of asymptomatic outpatients with cirrhosis and nonneutrocytic ascites. Liver Int 2011; 31: 494-498 [PMID:21382159 DOI:10.1111/j.1478-3231.2011.02448.x]
41. Feng Y, Chen CL, Chen TH, Liang YH, Chen HL, Lin CY, Chiu CH. Application of next-generation sequencing to study ascitic microbiome in cirrhotic patients with or without spontaneous bacterial peritonitis. J Microbiol Immunol Infect 2014; Epub ahead of print [PMID:25305707 DOI:10.1016/j.jmii.2014.07.005]
42. Fujita T. Is bacterial DNA a surrogate marker of bacterial translocation in cirrhosis? J Hepatol 2008; 49: 145-146; author reply 146-147 [PMID:18466995 DOI:10.1016/j.jhep.2008.04.001]
43. Vlachogiannakos J, Daikos G, Thalheimer U, Burroughs AK, Ladas SD. Is bacterial DNA a better marker than endotoxin of bacterial translocation in decompensated cirrhosis? Hepatology 2011; 53: 2140-2141; author reply 41-42 [PMID:21425309 DOI:10.1002/hep.24303]
44. Mortensen C, Jensen JS, Hobolth L, Dam-Larsen S, Madsen BS, Andersen O, Møller S, Bendtsen F. Association of markers of bacterial translocation with immune activation in decompensated cirrhosis. Eur J Gastroenterol Hepatol 2014; 26: 1360-1366 [PMID:25357217 DOI:10.1097/MEG.0000000000000217]
45. Mortensen C, Karlsen S, Grønbæk H, Nielsen DT, Frevert S, Clemmesen JO, Møller S, Jensen JS, Bendtsen F. No difference in portal and hepatic venous bacterial DNA in patients with cirrhosis undergoing transjugular intrahepatic portosystemic shunt insertion. Liver Int 2013; 33: 1309-1315 [PMID:23763259 DOI:10.1111/liv.12205]
46. Appenrodt B, Lehmann LE, Thyssen L, Gentemann M, Rabe C, Molitor E, Trebicka J, Stüber F, Sauerbruch T. Is detection of bacterial DNA in ascitic fluid of clinical relevance? Eur J Gastroenterol Hepatol 2010; 22: 1487-1494 [PMID:21048463 DOI:10.1097/MEG.0b013e328340c43a]
47. Frey EA, Miller DS, Jahr TG, Sundan A, Bazil V, Espevik T, Finlay BB, Wright SD. Soluble CD14 participates in the response of cells to lipopolysaccharide. J Exp Med 1992; 176: 1665-1671 [PMID:1281215]
48. Pugin J, Schürer-Maly CC, Leturcq D, Moriarty A, Ulevitch RJ, Tobias PS. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc Natl Acad Sci USA 1993; 90: 2744-2748 [PMID:7681988 DOI:10.1073/pnas.90.7.2744]
49. Heumann D, Roger T. Initial responses to endotoxins and Gramnegative bacteria. Clin Chim Acta 2002; 323: 59-72 [PMID:12135807 DOI:10.1016/S0009-8981(02)00180-8]
50. Le Roy D, Di Padova F, Adachi Y, Glauser MP, Calandra T, Heumann D. Critical role of lipopolysaccharide-binding protein and CD14 in immune responses against gram-negative bacteria. J Immunol 2001; 167: 2759-2765 [PMID:11509620 DOI:10.4049/jimmunol.167.5.2759]
51. Paik YH, Schwabe RF, Bataller R, Russo MP, Jobin C, Brenner DA. Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 2003; 37: 1043-1055 [PMID:12717385 DOI:10.1053/jhep.2003.50182]
52. Hanck C, Rossol S, Böcker U, Tokus M, Singer MV. Presence of plasma endotoxin is correlated with tumour necrosis factor receptor levels and disease activity in alcoholic cirrhosis. Alcohol Alcohol 1998; 33: 606-608 [PMID:9872348 DOI:10.1093/alcalc/33.6.606]
53. Fukui H, Brauner B, Bode JC, Bode C. Plasma endotoxin concentrations in patients with alcoholic and non-alcoholic liver disease: reevaluation with an improved chromogenic assay. J Hepatol 1991; 12: 162-169 [PMID:2050995 DOI:10.1016/0168-8278(91)90933-3]
54. Lin RS, Lee FY, Lee SD, Tsai YT, Lin HC, Lu RH, Hsu WC, Huang CC, Wang SS, Lo KJ. Endotoxemia in patients with chronic liver diseases: relationship to severity of liver diseases, presence of esophageal varices, and hyperdynamic circulation. J Hepatol 1995; 22: 165-172 [PMID:7790704 DOI:10.1016/0168-8278(95)80424-2]
55. Chan CC, Hwang SJ, Lee FY, Wang SS, Chang FY, Li CP, Chu CJ, Lu RH, Lee SD. Prognostic value of plasma endotoxin levels in patients with cirrhosis. Scand J Gastroenterol 1997; 32: 942-946 [PMID:9299675 DOI:10.3109/00365529709011206]
56. Kaser A, Ludwiczek O, Waldenberger P, Jaschke W, Vogel W, Tilg H. Endotoxin and its binding proteins in chronic liver disease: the effect of transjugular intrahepatic portosystemic shunting. Liver 2002; 22: 380-387 [PMID:12390473 DOI:10.1034/j.1600-0676.2002.01666.x]
57. Stadlbauer V, Davies NA, Wright G, Jalan R. Endotoxin measures in patients' sample: how valid are the results? J Hepatol 2007; 47: 726-727; author reply 727-723 [PMID:17850915 DOI:10.1016/j.jhep.2007.08.001]
58. Schumann RR, Kirschning CJ, Unbehaun A, Aberle HP, Knope HP, Lamping N, Ulevitch RJ, Herrmann F. The lipopolysaccharidebinding protein is a secretory class 1 acute-phase protein whose gene is transcriptionally activated by APRF/STAT/3 and other cytokine-inducible nuclear proteins. Mol Cell Biol 1996; 16: 3490-3503 [PMID:8668165]
59. Albillos A, de-la-Hera A, Alvarez-Mon M. Serum lipopolysaccharide-binding protein prediction of severe bacterial infection in cirrhotic patients with ascites. Lancet 2004; 363: 1608-1610 [PMID:15145636 DOI:10.1016/S0140-6736(04)16206-5]
60. Myc A, Buck J, Gonin J, Reynolds B, Hammerling U, Emanuel D. The level of lipopolysaccharide-binding protein is significantly increased in plasma in patients with the systemic inflammatory response syndrome. Clin Diagn Lab Immunol 1997; 4: 113-116 [PMID:9067641]
61. Landmann R, Knopf HP, Link S, Sansano S, Schumann R, Zimmerli W. Human monocyte CD14 is upregulated by lipopolysaccharide. Infect Immun 1996; 64: 1762-1769 [PMID:8613389]
62. Tuomisto S, Pessi T, Collin P, Vuento R, Aittoniemi J, Karhunen PJ. Changes in gut bacterial populations and their translocation into liver and ascites in alcoholic liver cirrhotics. BMC Gastroenterol 2014; 14: 40 [PMID:24564202 DOI:10.1186/1471-230X-14-40]
63. Sandler NG, Koh C, Roque A, Eccleston JL, Siegel RB, Demino M, Kleiner DE, Deeks SG, Liang TJ, Heller T, Douek DC. Host response to translocated microbial products predicts outcomes of patients with HBV or HCV infection. Gastroenterology 2011; 141: 1220-1230, 1230.e1-3 [PMID:21726511 DOI:10.1053/j.gastro.2011.06.063]
64. Balagopal A, Philp FH, Astemborski J, Block TM, Mehta A, Long R, Kirk GD, Mehta SH, Cox AL, Thomas DL, Ray SC. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology 2008; 135: 226-233 [PMID:18457674 DOI:10.1053/j.gastro.2008.03.022]
65. French AL, Evans CT, Agniel DM, Cohen MH, Peters M, Landay AL, Desai SN. Microbial translocation and liver disease progression in women coinfected with HIV and hepatitis C virus. J Infect Dis 2013; 208: 679-689 [PMID:23687224 DOI:10.1093/infdis/jit225]
66. Ogawa Y, Imajo K, Yoneda M, Kessoku T, Tomeno W, Shinohara Y, Kato S, Mawatari H, Nozaki Y, Fujita K, Kirikoshi H, Maeda S, Saito S, Wada K, Nakajima A. Soluble CD14 levels reflect liver inflammation in patients with nonalcoholic steatohepatitis. PLoS One 2013; 8: e65211 [PMID:23762319 DOI:10.1371/journal.pone.0065211]
67. Campos J, Gonzalez-Quintela A, Quinteiro C, Gude F, Perez LF, Torre JA, Vidal C. The -159C/T polymorphism in the promoter region of the CD14 gene is associated with advanced liver disease and higher serum levels of acute-phase proteins in heavy drinkers. Alcohol Clin Exp Res 2005; 29: 1206-1213 [PMID:16046876 DOI:10.1097/01.ALC.0000171977.25531.7A]
68. Fagerhol MK. Calprotectin, a faecal marker of organic gastrointestinal abnormality. Lancet 2000; 356: 1783-1784 [PMID:11117904 DOI:10.1016/S0140-6736(00)03224-4]
69. Johne B, Fagerhol MK, Lyberg T, Prydz H, Brandtzaeg P, Naess-Andresen CF, Dale I. Functional and clinical aspects of the myelomonocyte protein calprotectin. Mol Pathol 1997; 50: 113-123 [PMID:9292145 DOI:10.1136/mp.50.3.113]
70. Vermeire S, Van Assche G, Rutgeerts P. Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut 2006; 55: 426-431 [PMID:16474109 DOI:10.1136/gut.2005.069476]
71. KonikoffMR, Denson LA. Role of fecal calprotectin as a biomarker of intestinal inflammation in inflammatory bowel disease. Inflamm Bowel Dis 2006; 12: 524-534 [PMID:16775498 DOI:10.1097/00054725-200606000-00013]
72. Burri E, Beglinger C. The use of fecal calprotectin as a biomarker in gastrointestinal disease. Expert Rev Gastroenterol Hepatol 2014; 8: 197-210 [PMID:24345070 DOI:10.1586/17474124.2014.869476]
73. Sipponen T. Diagnostics and prognostics of inflammatory bowel disease with fecal neutrophil-derived biomarkers calprotectin and lactoferrin. Dig Dis 2013; 31: 336-344 [PMID:24246984 DOI:10.1159/000354689]
74. Homann C, Garred P, Graudal N, Hasselqvist P, Christiansen M, Fagerhol MK, Thomsen AC. Plasma calprotectin: a new prognostic marker of survival in alcohol-induced cirrhosis. Hepatology 1995; 21: 979-985 [PMID:7705809 DOI:10.1002/hep.1840210415]
75. Homann C, Christensen E, Schlichting P, Philipsen EK, Graudal NA, Garred P. Ascites fluid and plasma calprotectin concentrations in liver disease. Scand J Gastroenterol 2003; 38: 415-420 [PMID:12739714 DOI:10.1080/00365520310000870]
76. Homann C, Garred P, Graudal NA, Hasselqvist P, Christiansen M, Fagerhol MK, Thomsen AC. [Plasma calprotectin. A new prognostic marker of survival in alcoholic liver cirrhosis]. Ugeskr Laeger 1996; 158: 2980-2984 [PMID:8686035]
77. Gundling F, Schmidtler F, Hapfelmeier A, Schulte B, Schmidt T, Pehl C, Schepp W, Seidl H. Fecal calprotectin is a useful screening parameter for hepatic encephalopathy and spontaneous bacterial peritonitis in cirrhosis. Liver Int 2011; 31: 1406-1415 [PMID:22093455 DOI:10.1111/j.1478-3231.2011.02577.x]
78. Montalto M, Gallo A, Ferrulli A, Visca D, Campobasso E, Cardone S, D'Onofrio F, Santoro L, Covino M, Mirijello A, Leggio L, Gasbarrini G, Addolorato G. Fecal calprotectin concentrations in alcoholic patients: a longitudinal study. Eur J Gastroenterol Hepatol 2011; 23: 76-80 [PMID:21030869 DOI:10.1097/MEG.0b013e32834101f9]
79. Burri E, Schulte F, Muser J, Meier R, Beglinger C. Measurement of calprotectin in ascitic fluid to identify elevated polymorphonuclear cell count. World J Gastroenterol 2013; 19: 2028-2036 [PMID:23599621 DOI:10.3748/wjg.v19.i13.2028]
80. Alempijevic T, Štulic M, Popovic D, Culafic D, Dragasevic S, Milosavljevic T. The role of fecal calprotectin in assessment of hepatic encephalopathy in patients with liver cirrhosis. Acta Gastroenterol Belg 2014; 77: 302-305 [PMID:25509200]
81. Lutz P, Pfarr K, Nischalke HD, Krämer B, Goeser F, Glässner A, Wolter F, Kokordelis P, Nattermann J, Sauerbruch T, Hoerauf A, Strassburg CP, Spengler U. The ratio of calprotectin to total protein as a diagnostic and prognostic marker for spontaneous bacterial peritonitis in patients with liver cirrhosis and ascites. Clin Chem Lab Med 2015; Epub ahead of print [PMID:26035112 DOI:10.1515/cclm-2015-0284]
82. Montalto M, Gallo A, Santoro L, D'Onofrio F, LandolfiR, Gasbarrini A. Role of fecal calprotectin in gastrointestinal disorders. Eur Rev Med Pharmacol Sci 2013; 17: 1569-1582 [PMID:23832721]
83. Assink-de Jong E, de Lange DW, van Oers JA, Nijsten MW, Twisk JW, Beishuizen A. Stop Antibiotics on guidance of Procalcitonin Study (SAPS): a randomised prospective multicenter investigator-initiated trial to analyse whether daily measurements of procalcitonin versus a standard-of-care approach can safely shorten antibiotic duration in intensive care unit patients- calculated sample size: 1816 patients. BMC Infect Dis 2013; 13:
84. Bota DP, Van Nuffelen M, Zakariah AN, Vincent JL. Serum levels of C-reactive protein and procalcitonin in critically ill patients with cirrhosis of the liver. J Lab Clin Med 2005; 146: 347-351 [PMID:16310518 DOI:10.1016/j.lab.2005.08.005]
85. Connert S, Stremmel W, Elsing C. Procalcitonin is a valid marker of infection in decompensated cirrhosis. Z Gastroenterol 2003; 41: 165-170 [PMID:12592597 DOI:10.1055/s-2003-37314]
86. Cai ZH, Fan CL, Zheng JF, Zhang X, Zhao WM, Li B, Li L, Dong PL, Ding HG. Measurement of serum procalcitonin levels for the early diagnosis of spontaneous bacterial peritonitis in patients with decompensated liver cirrhosis. BMC Infect Dis 2015; 15: 55 [PMID:25887691 DOI:10.1186/s12879-015-0776-4]
87. Marciano S, Haddad L, Martínez AP, Posadas ML, Piñero F, Mora GJ, Guerrero LN, Ridruejo E, Mandó OG, Giunta DH, Gadano AC. Ultra-sensitive procalcitonin may help rule out bacterial infections in patients with cirrhosis. Ann Hepatol 2014; 13: 541-547 [PMID:25152987]
88. Lesinska M, Hartleb M, Gutkowski K, Nowakowska-Dulawa E. Procalcitonin and macrophage inflammatory protein-1 beta (MIP- 1β) in serum and peritoneal fluid of patients with decompensated cirrhosis and spontaneous bacterial peritonitis. Adv Med Sci 2014; 59: 52-56 [PMID:24797975 DOI:10.1016/j.advms.2013.07.006]
89. Cekin Y, Cekin AH, Duman A, Yilmaz U, Yesil B, Yolcular BO. The role of serum procalcitonin levels in predicting ascitic fluid infection in hospitalized cirrhotic and non-cirrhotic patients. Int J Med Sci 2013; 10: 1367-1374 [PMID:23983598 DOI:10.7150/ijms.6014]
90. Su DH, Zhuo C, Liao K, Cheng WB, Cheng H, Zhao XF. Value of serum procalcitonin levels in predicting spontaneous bacterial peritonitis. Hepatogastroenterology 2013; 60: 641-646 [PMID:23159389 DOI:10.5754/hge12645]
91. Li CH, Yang RB, Pang JH, Chang SS, Lin CC, Chen CH, Chen HY, Chiu TF. Procalcitonin as a biomarker for bacterial infections in patients with liver cirrhosis in the emergency department. Acad Emerg Med 2011; 18: 121-126 [PMID:21276124 DOI:10.1111/j.1553-2712.2010.00991.x]
92. Spahr L, Morard I, Hadengue A, Vadas L, Pugin J. Procalcitonin is not an accurate marker of spontaneous bacterial peritonitis in patients with cirrhosis. Hepatogastroenterology 2001; 48: 502-505 [PMID:11379342]
93. Viallon A, Zeni F, Pouzet V, Lambert C, Quenet S, Aubert G, Guyomarch S, Tardy B, Bertrand JC. Serum and ascitic procalcitonin levels in cirrhotic patients with spontaneous bacterial peritonitis: diagnostic value and relationship to pro-inflammatory cytokines. Intensive Care Med 2000; 26: 1082-1088 [PMID:11030164 DOI:10.1007/s001340051321]
94. Elefsiniotis IS, Skounakis M, Vezali E, Pantazis KD, Petrocheilou A, Pirounaki M, Papatsibas G, Kontou-Kastellanou C, Moulakakis A. Clinical significance of serum procalcitonin levels in patients with acute or chronic liver disease. Eur J Gastroenterol Hepatol 2006; 18: 525-530 [PMID:16607149 DOI:10.1097/00042737-200605000-00012]
95. Rahimkhani M, Einollahi N, Khavari Daneshvar H, Dashti N. Survey of serum procalcitonin in cirrhotic patients. Acta Med Iran 2013; 51: 153-156 [PMID:23605598]
96. Villarreal E, Vacacela K, Gordon M, Calabuig C, Alonso R, Ruiz J, Kot P, Babiloni D, Ramírez P. Usefulness of procalcitonin for diagnosing infection in critically ill patients with liver cirrhosis. Med Intensiva 2015; Epub ahead of print [PMID:25843699 DOI:10.1016/j.medin.2015.02.006]
97. Attar BM, Moore CM, George M, Ion-Nedelcu N, Turbay R, Zachariah A, Ramadori G, Fareed J, Van Thiel DH. Procalcitonin, and cytokines document a dynamic inflammatory state in noninfected cirrhotic patients with ascites. World J Gastroenterol 2014; 20: 2374-2382 [PMID:24605035 DOI:10.3748/wjg.v20.i9.2374]
98. Lazzarotto C, Ronsoni MF, Fayad L, Nogueira CL, Bazzo ML, Narciso-Schiavon JL, de Lucca Schiavon L, Dantas-Corrêa EB. Acute phase proteins for the diagnosis of bacterial infection and prediction of mortality in acute complications of cirrhosis. Ann Hepatol 2013; 12: 599-607 [PMID:23813138]
99. Papp M, Sipeki N, Vitalis Z, Tornai T, Altorjay I, Tornai I, Udvardy M, Fechner K, Jacobsen S, Teegen B, Sumegi A, Veres G, Lakatos PL, Kappelmayer J, Antal-Szalmas P. High prevalence of IgA class anti-neutrophil cytoplasmic antibodies (ANCA) is associated with increased risk of bacterial infection in patients with cirrhosis. J Hepatol 2013; 59: 457-466 [PMID:23639483 DOI:10.1016/j.jhep.2013.04.018]