• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of wjgLink to Publisher's site
World J Gastroenterol. Mar 7, 2009; 15(9): 1042–1049.
Published online Mar 7, 2009. doi:  10.3748/wjg.15.1042
PMCID: PMC2655193

Spontaneous bacterial peritonitis

Abstract

Since its initial description in 1964, research has transformed spontaneous bacterial peritonitis (SBP) from a feared disease (with reported mortality of 90%) to a treatable complication of decompensated cirrhosis, albeit with steady prevalence and a high recurrence rate. Bacterial translocation, the key mechanism in the pathogenesis of SBP, is only possible because of the concurrent failure of defensive mechanisms in cirrhosis. Variants of SBP should be treated. Leucocyte esterase reagent strips have managed to shorten the ‘tap-to-shot’ time, while future studies should look into their combined use with ascitic fluid pH. Third generation cephalosporins are the antibiotic of choice because they have a number of advantages. Renal dysfunction has been shown to be an independent predictor of mortality in patients with SBP. Albumin is felt to reduce the risk of renal impairment by improving effective intravascular volume, and by helping to bind pro-inflammatory molecules. Following a single episode of SBP, patients should have long-term antibiotic prophylaxis and be considered for liver transplantation.

Keywords: Spontaneous bacterial peritonitis, Infection, Ascites, Leucocyte reagent strips, Portal hypertension, Ascites

INTRODUCTION

It seems that all diseases or syndromes that comprise our routine differential diagnoses were, not so long ago, obscure clinical entities, at least until an astute clinician came across them. It was not any different for spontaneous bacterial peritonitis (SBP).

Although Laënnec’s name had been connected with cirrhosis since the early 1800s, it was only much later that SBP was diagnosed as a separate entity. The papers of Kerr et al[1] and Conn[2], which were published within a year of each other, describe the infection of ascitic fluid in the absence of a contiguous source of infection or an intra-abdominal inflammatory focus. Although similar reports had been published in the French literature since 1893, Conn[2] was the one who eventually coined the term (SBP) in his 1964 paper.

Since then, further research has made the once-feared disease (early reported mortality of 90%)[2] a treatable complication of decompensated cirrhosis[3], albeit with a steady prevalence and high recurrence rate[4,5]. The plethora of publications has also led to national/international guidelines and recommendations over the last 10 years[511].

PATHOGENESIS

The importance of the liver as a bacterial filter is well established. However, it was Conn[2] who hypothesized that intestinal bacteria escaping into the blood stream cause prolonged bacteremia, and in turn, a greater chance of ascitic fluid invasion[3]. Other early reports have emphasized the possibility of abdominal paracentesis-induced SBP[1,3], and certainly, prior to the use of stringent skin disinfection and protective clothing, the incidence of paracentesis-induced peritonitis would have been higher. The negative impact of this thinking created generations of clinicians who were hesitant and unsure about dealing with infective ascites. The persistence of researchers has helped to assuage concerns and has led to a more liberal and appropriate paracentesis protocol[1214].

Bacterial translocation (BT), the key mechanism in the pathogenesis of SBP, is only possible because of the concurrent failure of defensive mechanisms in cirrhosis[1519]. Since the early 1990s, on-going research has confirmed the intensity of BT in cirrhotic rats[1521]. Investigators have also demonstrated pronounced impairment of gastrointestinal tract motility in cirrhosis[2224]. The disturbance of gut flora microecology that follows, in association with changes in the (ultra)structure of the gastrointestinal tract[2527] and reduced local and humoral immunity paves the way for the relatively free flow of microorganisms and/or endotoxins to the mesenteric lymph nodes[2527].

CLINICAL MANIFESTATIONS OF SBP

The clinical manifestations of SBP are subtle and require a high index of suspicion (Table (Table1).1). Previously, there was often delay in diagnosis, which led to considerable mortality and morbidity[28].

Table 1
Symptoms and signs of ascitic fluid infection

SBP almost always occurs in large volume ascites, in patients with liver cirrhosis. Ascites of other causes or low volume rarely gives rise to SBP. Patients with cirrhosis usually have hypothermia; therefore, any temperature > 37.8°C should be investigated, unless it is clearly caused by flu-like symptoms. The necessary investigations are full blood count (FBC), urinalysis, ascitic fluid cell count, and ascites, blood and urine culture. Fever caused by SBP is differentiated from that of alcoholic hepatitis, in which the ascitic fluid neutrophil count is normal[28]. Alterations in mental status may be subtle and only apparent to someone close to the patient. A connect-the-number test, e.g. Reitan trail test, is preferable to testing serum ammonia levels[29]. Abdominal pain can be continuous and is different from tense ascites. Tenderness is a common feature. Paralytic ileus, hypotension and hypothermia are seen in advanced illness, where prognosis may be dire. Thirteen percent of patients have no signs or symptoms[28]. A ‘diagnostic tap’ should be performed in all patients with ascites admitted to hospital. SBP in outpatients with cirrhotic ascites is less frequent, occurs in patients with less advanced liver disease, and may have a better outcome than its counterpart in hospitalized patients[30]. A retrospective review of 916 outpatient AF samples from the United States showed that abnormal AF appearance had a sensitivity of 98.1% [(95% confidence interval (CI): 95.3%-99.5%] and a specificity of 22.7% (95% CI: 19.4%-26.3%) in the detection of SBP[31]. For out- and inpatients, laboratory abnormalities such as leukocytosis, metabolic acidosis and azotemia, should prompt investigations for SBP, even in the absence of other clinical features.

TECHNIQUES AND LABORATORY DIAGNOSIS

The process of ascitic fluid analysis has come a long way. Inspections for color and transparency (as first evidence of infection) will probably always be carried out. Practice from this point forward, however, varies between regions and to a lesser extent, between hospitals. Over the last decade, it seems that a selective, possibly common-sense approach has started to prevail over the light-hearted dictum “send it (AF) for everything”.

The diagnostic algorithm proposed by Runyon[28] (Figure (Figure1)1) remains the most logical and cost-effective way to handle an abdominal paracentesis specimen, and we recommend that every gastrointestinal (GI) ward should have a laminated copy readily available in the doctors’ office or protocol folder. Diagnostic paracentesis is now regarded as a safe procedure. Undoubtedly, there are complications inherent with the test, but the incidence rate of these is low[3234]. The reported risks of diagnostic paracentesis include bleeding (hemoperitoneum or abdominal wall hematoma), visceral perforation, local infection at the site of paracentesis, or peritonitis. However, the most common complication is persistent leak. Post-procedural bleeding risk is very low, not only for diagnostic, but also for therapeutic taps[3336]. Runyon has suggested that the practice of attempting to correct any coagulopathy prior to paracentesis is not cost-effective[28]. The use of trans-abdominal ultrasound (TUS) assists in a more accurate AF tap; therefore, it is an appealing alternative to the blind technique[3739].

Figure 1
Algorithm for diffe-rentiating spontaneous from secondary bacterial peritonitis in patients with neutrocytic ascites (i.e. neutrophil count of 250 cells/mm3 or greater) in the absence of hemorrhage into ascitic fluid, tuberculosis, peritoneal carcinomatosis, ...

The majority of the inpatient diagnostic AF taps are performed with a blind technique. The accepted area of preference is away from the midline, at the point of maximal dullness, and ideally in the left iliac fossa, two fingerbreadths medial and two ventral to the anterior superior iliac spine (“Runyon’s spot”)[28]. We advise that after two dry taps, TUS should be used to mark the best insertion spot. Equipment required for the tap comprises: 10-mL syringe; 1.5-inch, 22-gauge metal (or 18-gauge) needle; pack of sterile gloves and a galipot with skin disinfectant[34,40]. Thirty milliliters of ascitic fluid should be aspirated and distributed between two blood culture bottles (aerobic and anaerobic, ideally 5-10 mL in each after replacement of the paracentesis green needle by a sterile one), a purple top tube and a brown top one for the necessary biochemistry.

The biochemical tests required for every ascitic fluid sample are for protein, albumin, glucose and lactate dehydrogenase, while other tests are graded between optional and unnecessary. Further expansion on AF biochemistry is beyond the scope of this review and the reader is advised to consult relevant textbooks/reviews[28]. Reference will only be made to AF tests used for the diagnosis of SBP.

A review of the laboratory diagnosis of SBP would not be complete without alluding to the most recent and practical change in protocol. Following aspiration of the AF sample, after inoculating the culture bottles and prior to splitting the rest of the sample into the purple- and brown-topped tubes, a small amount should be poured over a leukocyte esterase reagent strip (LERS) (any urine dipstick has the relevant reagent square), in order to detect any color change in the respective square. The colorimetric scale reference chart can be viewed on the side of the storage container. Results are obtained by direct optical comparison of the LERS with the scale, or, when available, by spectrophotometric analysis. Hepatologists, gastroenterologists and internists have developed an interest in this new addition (at least for AF analysis), especially as satisfactory sensitivity and specificity for SBP detection have been reported in small French and Spanish studies[4143]. Further studies have been conducted worldwide[4448]. However, initial enthusiasm and suggestions that LERSs may be used as the sole method of detection of AF infection have been tempered by the latest reports and two systematic reviews[4951]. It appears that enthusiasm alone replaced structured, evidence-based approaches for LERSs in the presumptive diagnosis of SBP[50,51].

In rural, remote and smaller hospitals and in developing countries, LERSs shrink the ‘tap-to-shot’ time i.e. the time between paracentesis and first antibiotic dose, to only a few minutes. LERSs bear no resemblance to pH, lactate, lactoferrin or other difficult-to-measure infection indices. However, they are cheap and readily available. Moreover, no diagnosis is made in a clinical vacuum and in the right clinical context, the use of a single ‘stat’ dose prompted by a positive LERS can potentially lessen the burden of infection[5153].

Eventually, the AF sample will find its way to the bench of a busy clinical laboratory. It is known that in SBP, the number of polymorphonuclear neutrophils (PMNs) in the ascitic fluid is ≥ 250/mL[6,28]. Despite numerous publications emphasizing the contrary[13,28,54,55], many AF samples are prioritized inappropriately by clinical laboratories, giving rise to a significant delay in results. The manual count (performed by the traditional hematological method utilizing a microscope and Bucker chamber) is laborious and, in many instances, subjective. Angeloni et al[56] have produced clinical evidence that manual and automated PMN counting is equally efficient[57]. Cereto et al[58] have confirmed these results. Two years later, Link and colleagues (prompted by the statement of the International Ascites Club consensus document) examined the use of automated counters in detecting the total leucocyte count in ascitic fluid and diagnosing SBP[59]. It is surprising that such a crucial issue in expediting the diagnosis of SBP remained unaddressed for so long by many laboratories, which, despite the above evidence, continued to employ the old-fashioned manual technique over the automated one. At this point, it is necessary to highlight an important caveat when determining AF PMN count: an accurate PMN count may only be determined after non-traumatic paracentesis. If the tap is traumatic or the fluid is a priori hemorrhagic (red cells ≥ 10 000/mL), the PMN count should be corrected as follows: subtract (from the measured PMN count) 1 PMN for every 250 red cells[7].

Opinion is still divided on the issue of automated vs manual testing, but utilization of culture bottles in SBP diagnosis is now the well-established gold standard. SBP is a low-colony-count, monomicrobial infection of the AF and, in this context, is very similar to bacteremia. The use of blood culture bottles can increase the yield of AF culture from 40% to > 80%[7].

Although initially attractive[60], pH testing of the AF, has now fallen into obscurity[28,34]. This is partly attributable to limited clinical accessibility and partly to increased investigator interest in newer measurements, i.e. procalcitonin and lactoferrin[4,60]. pH was last used in a clinical study in 1995[34]. In their systematic review, Wong et al[34] have found that ascitic fluid pH ≤ 7.35 and blood-ascitic fluid odds ratio (OR) ≥ 0.10 had the highest diagnostic OR for SBP, and it may be reasonable to suggest a return to pH testing combined with LERSs as an appropriate means to diagnose SBP. The majority of urine dipsticks include a pH reagent square and the latest study on the subject has demonstrated that combination of LERSs with nitrite offers no additional benefit in SBP detection[48]. As far as we are aware, no study has investigated the combination of pH squares with LERSs. We can, however, envisage similar problems to those experienced by investigators in LERS studies occurring in this instance, namely, the lack of specificity of the reagents used for the usual pH values of AF (urine pH reference range is 6.75-7.5).

The use of procalcitonin should also be mentioned. Procalcitonin is the pro-hormone of calcitonin. It is synthesized in many different tissues of infected organs and has been hailed as a novel index of inflammation. Initial interest in its use in SBP[61] was eventually dampened by another study a year later[62]. Lactoferrin seems far more promising to serve as a rapid and reliable screening tool for SBP in patients with cirrhosis, and a recent study has suggested the need to develop an AF-specific dipstick[63].

SBP VARIANTS

Bacterascites (monomicrobial non-neutrocytic bacterascites) is the term used to describe the colonization of ascitic fluid by bacteria, in the absence of an inflammatory reaction in the bacterial fluid. By definition, the PMN count is < 250/mm3 and bacterial culture is positive, while the patient may present with symptoms and signs of infection. The natural course of bacterascites, if untreated, is variable. Diagnosis of bacterascites can only be made 2-3 d after initial paracentesis (the time necessary for culture growth), and a repeat ascitic tap is recommended on day 3. If the second sample has a PMN count > 250/mm3, the current recommendation is to treat as for SBP. If the PMN count is < 250/mm3, but the second set of cultures is positive, treat again as for SBP. If the PMN count is < 250/mm3 and the second set of cultures is negative, no further action is recommended[7,28].

Culture-negative neutrocytic ascites is the term used to describe the clinical situation in which the ascitic PMN count is > 250/mm3 but fluid cultures fail to grow any bacteria. It is considered to represent the expected 20% failure rate of culture to isolate microorganisms, and it requires antibiotic treatment as if it were SBP. However, the term is now considered obsolete[28,55].

MANAGEMENT

Appropriate antibiotic therapy should achieve resolution of infection in most cases of SBP[64]. However, the management of SBP is complex and not just a matter of empirical therapy. Important issues include: (1) identification of the underlying organism; (2) choice of safe and appropriate antibiotics; (3) preservation of renal function and treatment of renal dysfunction; (4) duration of antibiotic therapy; and (5) subsequent antibiotic prophylaxis.

Whilst clarifying the diagnosis of SBP with paracentesis, an attempt should be made at identification of the underlying organism with inoculation of ascitic fluid into blood culture bottles. This vastly improves the identification of the responsible organism and, therefore, allows improved treatment of atypical or resistant organisms. Inoculation into blood culture bottles improves diagnostic yield from 40% to around 80%[65]. Simultaneous blood cultures should be taken as 50% of cases of SBP are associated with bacteremia[66].

The common causative organisms of SBP are Gram-negative bacteria such as Escherichia coli and other coliforms such as Klebsiella spp. These account for at least 50% of cases. Other causative organisms include pneumococci, streptococci and miscellaneous Gram-positive and -negative organisms[28,55,65,66] (Table (Table22).

Table 2
Pathogens in ascitic fluid infection

Empirical therapy should not be delayed (beyond the first few minutes needed for LERS reading) while awaiting identification of the exact organism. Third generation cephalosporins are the antibiotic of choice as they have a number of advantages: (1) relatively safe and well tolerated; (2) broad spectrum activity; and (3) effectiveness, with many studies confirming high levels of SBP resolution.

Cefotaxime 2 g every 12 h is often used intravenously for at least 5 d[6769]. A 5-d course of treatment has been shown to be equally effective as 10 d[70]. Other third generation cephalosporins (e.g. ceftriaxone) are felt to be equally effective[3,7173]. Alternative antibiotic regimens include amoxycillin/clavulanic acid, fluoroquinolones or piperacillin/tazobactam[7477] (Table (Table3).3). Regional resistance patterns should be accounted for with early communication with a microbiologist if necessary[11,77]. According to the International Ascites Club, it is important to perform a second tap 48 h after the start of therapy. If there is a less than a 25% drop in PMN count from baseline, a change of antibiotic should be considered[4,5].

Table 3
Costs of antibiotics used for spontaneous bacterial peritonitis

Renal function

One third of patients with SBP will develop renal failure. The renal dysfunction is thought to occur as a result of a reduced effective circulating volume[7,78]. Renal dysfunction has been shown to be an independent predictor of mortality in patients with SBP[79]. Therefore, close attention to renal function and the avoidance of nephrotoxic medication is paramount. On the other hand, diuretic therapy and large-volume paracentesis should not be necessarily withheld (they potentially exacerbate the reduction in effective circulating volume and contribute to renal deterioration) if albumin is administered[80,81]. The benefit of human albumin solution for treating renal dysfunction has been studied in randomized controlled trials[82,83]. Albumin is thought to reduce the risk of renal impairment by improving effective intravascular volume and by helping to bind pro-inflammatory molecules[7,8,11]. Studies have shown an improvement in short-term survival and a reduction in renal impairment in patients with SBP treated with albumin. Although these studies have been subject to criticism[84,85], most authors agree that infusion of 1.5 g/kg on day 1 and 1 g/kg on day 3 is beneficial in patients that have developed, or are developing renal dysfunction[7,61]. Patients with normal renal function are unlikely to benefit from albumin therapy.

PROPHYLAXIS

Unfortunately, the long-term prognosis of patients with cirrhosis who have had a prior episode of SBP is poor. Mortality rates of 50%-70% have been reported at 1 year follow-up[7,11]. This is largely a result of the advanced stage of liver cirrhosis in these patients, along with the associated complications[86]. The recurrence rate of SBP following a first episode is up to 70% at 1 year[7,86]. Given the high recurrence rate, it seems sensible to recommend prophylaxis to this group of patients and referral for transplant assessment. This therapy is backed up by evidence showing a reduction in recurrence of SBP from 68% to 20% in one study[87].

Norfloxacin 400 mg/d or ciprofloxacin 500 mg/d orally appear to be the most studied and commonly recommended regimes[8792]. Levofloxacin or antibiotic cycling may be used as an alternative[9395]. There is debate over the use of antibiotics as primary prophylaxis against SBP. Some studies have shown reduced rates of SBP in selected patients deemed at high risk of developing SBP (those with low ascitic total protein)[79,91,96]. However, there are various criticisms of these studies, and at present, primary prophylaxis is not recommended. Further studies may help clarify this issue.

The last group of patients that are felt to benefit from antibiotic prophylaxis are those with known cirrhosis admitted with GI bleeding. Infection rates are high in this group regardless of whether they have ascites. The infection rates are also higher than those in patient with cirrhosis admitted for other reasons[61]. Several studies have shown a clear benefit from initiating antibiotic prophylaxis in this group[97100]. Reductions in infection rate and mortality have been noted. Once again, the choice of antibiotic should be broad spectrum and guided by local policy; either oral norfloxacin or ciprofloxacin have been suggested[7,61].

Peer reviewer: Diego Garcia-Compean, MD, Professor, Faculty of Medicine, University Hospital, Department of Gastroenterology, Autonomous University of Nuevo Leon, Ave Madero y Gonzalitos, 64700 Monterrey, N.L. Mexico

S- Editor Tian L L- Editor Kerr C E- Editor Zheng XM

References

1. Kerr DN, Pearson DT, Read AE. Infection of ascitic fluid in patients with hepatic cirrhosis. Gut. 1963;4:394–398. [PMC free article] [PubMed]
2. Conn HO. Spontaneous peritonitis and bacteremia in laennec’s cirrhosis caused by enteric organisms. A relatively common but rarely recognized syndrome. Ann Intern Med. 1964;60:568–580. [PubMed]
3. Garcia-Tsao G. Spontaneous bacterial peritonitis: a historical perspective. J Hepatol. 2004;41:522–527. [PubMed]
4. Angeloni S, Leboffe C, Parente A, Venditti M, Giordano A, Merli M, Riggio O. Efficacy of current guidelines for the treatment of spontaneous bacterial peritonitis in the clinical practice. World J Gastroenterol. 2008;14:2757–2762. [PMC free article] [PubMed]
5. Wong F, Bernardi M, Balk R, Christman B, Moreau R, Garcia-Tsao G, Patch D, Soriano G, Hoefs J, Navasa M. Sepsis in cirrhosis: report on the 7th meeting of the International Ascites Club. Gut. 2005;54:718–725. [PMC free article] [PubMed]
6. Salerno F, Angeli P, Bernardi M, Laffi G, Riggio O, Salvagnini M. Clinical practice guidelines for the management of cirrhotic patients with ascites. Committee on Ascites of the Italian Association for the Study of the Liver. Ital J Gastroenterol Hepatol. 1999;31:626–634. [PubMed]
7. Rimola A, García-Tsao G, Navasa M, Piddock LJ, Planas R, Bernard B, Inadomi JM. Diagnosis, treatment and prophylaxis of spontaneous bacterial peritonitis: a consensus document. International Ascites Club. J Hepatol. 2000;32:142–153. [PubMed]
8. Runyon BA. Management of adult patients with ascites due to cirrhosis. Hepatology. 2004;39:841–856. [PubMed]
9. WGO practice guideline: Condition: Management of ascites complicating cirrhosis in adults. Available from: URL: http://www.worldgastroenterology.org/assets/downloads/en/pdf/guidelines/14_management_ascites_en.pdf
10. Peck-Radosavljevic M, Trauner M, Schreiber F. Austrian consensus on the definition and treatment of portal hypertension and its complications. Endoscopy. 2005;37:667–673. [PubMed]
11. Moore KP, Aithal GP. Guidelines on the management of ascites in cirrhosis. Gut. 2006;55 Suppl 6:vi1–v12. [PMC free article] [PubMed]
12. Hoefs JC, Runyon BA. Spontaneous bacterial peritonitis. Dis Mon. 1985;31:1–48. [PubMed]
13. Runyon BA. Spontaneous bacterial peritonitis: an explosion of information. Hepatology. 1988;8:171–175. [PubMed]
14. Runyon BA. Strips and tubes: improving the diagnosis of spontaneous bacterial peritonitis. Hepatology. 2003;37:745–747. [PubMed]
15. Runyon BA, Squier S, Borzio M. Translocation of gut bacteria in rats with cirrhosis to mesenteric lymph nodes partially explains the pathogenesis of spontaneous bacterial peritonitis. J Hepatol. 1994;21:792–796. [PubMed]
16. Llovet JM, Bartolí R, Planas R, Cabré E, Jimenez M, Urban A, Ojanguren I, Arnal J, Gassull MA. Bacterial translocation in cirrhotic rats. Its role in the development of spontaneous bacterial peritonitis. Gut. 1994;35:1648–1652. [PMC free article] [PubMed]
17. Garcia-Tsao G, Lee FY, Barden GE, Cartun R, West AB. Bacterial translocation to mesenteric lymph nodes is increased in cirrhotic rats with ascites. Gastroenterology. 1995;108:1835–1841. [PubMed]
18. Guarner C, Runyon BA, Young S, Heck M, Sheikh MY. Intestinal bacterial overgrowth and bacterial translocation in cirrhotic rats with ascites. J Hepatol. 1997;26:1372–1378. [PubMed]
19. Cirera I, Bauer TM, Navasa M, Vila J, Grande L, Taurá P, Fuster J, García-Valdecasas JC, Lacy A, Suárez MJ, et al. Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol. 2001;34:32–37. [PubMed]
20. Runyon BA, Sugano S, Kanel G, Mellencamp MA. A rodent model of cirrhosis, ascites, and bacterial peritonitis. Gastroenterology. 1991;100:489–493. [PubMed]
21. Sánchez E, Casafont F, Guerra A, de Benito I, Pons-Romero F. Role of intestinal bacterial overgrowth and intestinal motility in bacterial translocation in experimental cirrhosis. Rev Esp Enferm Dig. 2005;97:805–814. [PubMed]
22. Chesta J, Lillo R, Defilippi C, Jouanee E, Massone MA, Maulén M, Zavala A. [Patients with liver cirrhosis: mouth-cecum transit time and gastric emptying of solid foods] Rev Med Chil. 1991;119:1248–1253. [PubMed]
23. Madrid AM, Cumsille F, Defilippi C. Altered small bowel motility in patients with liver cirrhosis depends on severity of liver disease. Dig Dis Sci. 1997;42:738–742. [PubMed]
24. Madrid AM, Brahm J, Antezana C, González-Koch A, Defilippi C, Pimentel C, Oksenberg D, Defilippi C. Small bowel motility in primary biliary cirrhosis. Am J Gastroenterol. 1998;93:2436–2440. [PubMed]
25. Chiva M, Guarner C, Peralta C, Llovet T, Gómez G, Soriano G, Balanzó J. Intestinal mucosal oxidative damage and bacterial translocation in cirrhotic rats. Eur J Gastroenterol Hepatol. 2003;15:145–150. [PubMed]
26. Ramachandran A, Prabhu R, Thomas S, Reddy JB, Pulimood A, Balasubramanian KA. Intestinal mucosal alterations in experimental cirrhosis in the rat: role of oxygen free radicals. Hepatology. 2002;35:622–629. [PubMed]
27. Karahan OI, Dodd GD 3rd, Chintapalli KN, Rhim H, Chopra S. Gastrointestinal wall thickening in patients with cirrhosis: frequency and patterns at contrast-enhanced CT. Radiology. 2000;215:103–107. [PubMed]
28. Runyon BA. Ascites and spontaneous bacterial peritonitis. In: M Feldman, LS Friedman, MH Sleisenger., editors. Sleisenger and Fordran’s gastrointestinal and liver disease, 8th ed. Saunders: Philadelphia; 2006. pp. 1935–1964.
29. Conn HO. Trailmaking and number-connection tests in the assessment of mental state in portal systemic encephalopathy. Am J Dig Dis. 1977;22:541–550. [PubMed]
30. Evans LT, Kim WR, Poterucha JJ, Kamath PS. Spontaneous bacterial peritonitis in asymptomatic outpatients with cirrhotic ascites. Hepatology. 2003;37:897–901. [PubMed]
31. Chinnock B, Hendey GW. Can clear ascitic fluid appearance rule out spontaneous bacterial peritonitis? Am J Emerg Med. 2007;25:934–937. [PubMed]
32. Runyon BA. Paracentesis of ascitic fluid. A safe procedure. Arch Intern Med. 1986;146:2259–2261. [PubMed]
33. McGibbon A, Chen GI, Peltekian KM, van Zanten SV. An evidence-based manual for abdominal paracentesis. Dig Dis Sci. 2007;52:3307–3315. [PubMed]
34. Wong CL, Holroyd-Leduc J, Thorpe KE, Straus SE. Does this patient have bacterial peritonitis or portal hypertension? How do I perform a paracentesis and analyze the results? JAMA. 2008;299:1166–1178. [PubMed]
35. Pache I, Bilodeau M. Severe haemorrhage following abdominal paracentesis for ascites in patients with liver disease. Aliment Pharmacol Ther. 2005;21:525–529. [PubMed]
36. Grabau CM, Crago SF, Hoff LK, Simon JA, Melton CA, Ott BJ, Kamath PS. Performance standards for therapeutic abdominal paracentesis. Hepatology. 2004;40:484–488. [PubMed]
37. Bard C, Lafortune M, Breton G. Ascites: ultrasound guidance or blind paracentesis? CMAJ. 1986;135:209–210. [PMC free article] [PubMed]
38. Nazeer SR, Dewbre H, Miller AH. Ultrasound-assisted paracentesis performed by emergency physicians vs the traditional technique: a prospective, randomized study. Am J Emerg Med. 2005;23:363–367. [PubMed]
39. Sakai H, Sheer TA, Mendler MH, Runyon BA. Choosing the location for non-image guided abdominal paracentesis. Liver Int. 2005;25:984–986. [PubMed]
40. Thomsen TW, Shaffer RW, White B, Setnik GS. Videos in clinical medicine. Paracentesis. N Engl J Med. 2006;355:e21. [PubMed]
41. Vanbiervliet G, Rakotoarisoa C, Filippi J, Guérin O, Calle G, Hastier P, Mariné-Barjoan E, Schneider S, Piche T, Broussard JF, et al. Diagnostic accuracy of a rapid urine-screening test (Multistix8SG) in cirrhotic patients with spontaneous bacterial peritonitis. Eur J Gastroenterol Hepatol. 2002;14:1257–1260. [PubMed]
42. Castellote J, López C, Gornals J, Tremosa G, Fariña ER, Baliellas C, Domingo A, Xiol X. Rapid diagnosis of spontaneous bacterial peritonitis by use of reagent strips. Hepatology. 2003;37:893–896. [PubMed]
43. Thévenot T, Cadranel JF, Nguyen-Khac E, Tilmant L, Tiry C, Welty S, Merzoug N. Diagnosis of spontaneous bacterial peritonitis in cirrhotic patients by use of two reagent strips. Eur J Gastroenterol Hepatol. 2004;16:579–583. [PubMed]
44. Sapey T, Mena E, Fort E, Laurin C, Kabissa D, Runyon BA, Mendler MH. Rapid diagnosis of spontaneous bacterial peritonitis with leukocyte esterase reagent strips in a European and in an American center. J Gastroenterol Hepatol. 2005;20:187–192. [PubMed]
45. Braga LL, Souza MH, Barbosa AM, Furtado FM, Campelo PA, Araújo Filho AH. Diagnosis of spontaneous bacterial peritonitis in cirrhotic patients in northeastern Brazil by use of rapid urine-screening test. Sao Paulo Med J. 2006;124:141–144. [PubMed]
46. Li J, Pan Y, Bao WG, Niu JQ, Wang F. [Multistix10SG urine test in diagnosing spontaneous bacterial peritonitis] Zhonghua Ganzangbing Zazhi. 2006;14:784–785. [PubMed]
47. Rerknimitr R, Rungsangmanoon W, Kongkam P, Kullavanijaya P. Efficacy of leukocyte esterase dipstick test as a rapid test in diagnosis of spontaneous bacterial peritonitis. World J Gastroenterol. 2006;12:7183–7187. [PMC free article] [PubMed]
48. Torun S, Dolar E, Yilmaz Y, Keskin M, Kiyici M, Sinirtas M, Sarandol E, Gurel S, Nak SG, Gulten M. Evaluation of leukocyte esterase and nitrite strip tests to detect spontaneous bacterial peritonitis in cirrhotic patients. World J Gastroenterol. 2007;13:6027–6030. [PubMed]
49. Nousbaum JB, Cadranel JF, Nahon P, Khac EN, Moreau R, Thévenot T, Silvain C, Bureau C, Nouel O, Pilette C, Paupard T, Vanbiervliet G, Oberti F, Davion T, Jouannaud V, Roche B, Bernard PH, Beaulieu S, Danne O, Thabut D, Chagneau-Derrode C, de Lédinghen V, Mathurin P, Pauwels A, Bronowicki JP, Habersetzer F, Abergel A, Audigier JC, Sapey T, Grangé JD, Tran A. Diagnostic accuracy of the Multistix 8 SG reagent strip in diagnosis of spontaneous bacterial peritonitis. Hepatology. 2007;45:1275–1281. [PubMed]
50. Nguyen-Khac E, Cadranel JF, Thevenot T, Nousbaum JB. Review article: the utility of reagent strips in the diagnosis of infected ascites in cirrhotic patients. Aliment Pharmacol Ther. 2008;28:282–288. [PubMed]
51. Koulaouzidis A, Leontiadis GI, Abdullah M, Moschos J, Gasem J, Tharakan J, Maltezos E, Saeed AA. Leucocyte esterase reagent strips for the diagnosis of spontaneous bacterial peritonitis: a systematic review. Eur J Gastroenterol Hepatol. 2008;20:1055–1060. [PubMed]
52. Castellote J, Xiol X. Reagent strips and spontaneous bacterial peritonitis. Aliment Pharmacol Ther. 2008;28:660; author reply 661. [PubMed]
53. Sierra F, Torres D, Cárdenas A. The role of likelihood ratio in clinical diagnosis: applicability in the setting of spontaneous bacterial peritonitis. Clin Gastroenterol Hepatol. 2005;3:85–89. [PubMed]
54. Koulaouzidis A, Said E, Saeed AA. Use of urine dipsticks in spontaneous bacterial peritonitis (SBP): benefit for the busy junior physician [abstract] Endoscopy. 2006;38:1187.
55. Koulaouzidis A, Bhat S, Karagiannidis A, Tan WC, Linaker BD. Spontaneous bacterial peritonitis. Postgrad Med J. 2007;83:379–383. [PMC free article] [PubMed]
56. Angeloni S, Nicolini G, Merli M, Nicolao F, Pinto G, Aronne T, Attili AF, Riggio O. Validation of automated blood cell counter for the determination of polymorphonuclear cell count in the ascitic fluid of cirrhotic patients with or without spontaneous bacterial peritonitis. Am J Gastroenterol. 2003;98:1844–1848. [PubMed]
57. Riggio O, Angeloni S, Parente A, Leboffe C, Pinto G, Aronne T, Merli M. Accuracy of the automated cell counters for management of spontaneous bacterial peritonitis. World J Gastroenterol. 2008;14:5689–5694. [PMC free article] [PubMed]
58. Cereto F, Genescà J, Segura R. Validation of automated blood cell counters for the diagnosis of spontaneous bacterial peritonitis. Am J Gastroenterol. 2004;99:1400. [PubMed]
59. Link BC, Ziske CG, Schepke M, Schmidt-Wolf IG, Sauerbruch T. Total ascitic fluid leukocyte count for reliable exclusion of spontaneous bacterial peritonitis in patients with ascites. Eur J Gastroenterol Hepatol. 2006;18:181–186. [PubMed]
60. Stassen WN, McCullough AJ, Bacon BR, Gutnik SH, Wadiwala IM, McLaren C, Kalhan SC, Tavill AS. Immediate diagnostic criteria for bacterial infection of ascitic fluid. Evaluation of ascitic fluid polymorphonuclear leukocyte count, pH, and lactate concentration, alone and in combination. Gastroenterology. 1986;90:1247–1254. [PubMed]
61. 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. [PubMed]
62. 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. [PubMed]
63. Parsi MA, Saadeh SN, Zein NN, Davis GL, Lopez R, Boone J, Lepe MR, Guo L, Ashfaq M, Klintmalm G, et al. Ascitic fluid lactoferrin for diagnosis of spontaneous bacterial peritonitis. Gastroenterology. 2008;135:803–807. [PubMed]
64. Ghassemi S, Garcia-Tsao G. Prevention and treatment of infections in patients with cirrhosis. Best Pract Res Clin Gastroenterol. 2007;21:77–93. [PubMed]
65. Garcia-Tsao G. Spontaneous bacterial peritonitis. Gastroenterol Clin North Am. 1992;21:257–275. [PubMed]
66. Arroyo V, Bataller R, Ginès P. Spontaneous bacterial peritonitis. In: O’Grady IG, Lake JR, Howdle PD, editors. Comprehensive clinical hepatology. 1st ed. Mosby: Barcelona; 2000. pp. 153–169.
67. Felisart J, Rimola A, Arroyo V, Perez-Ayuso RM, Quintero E, Gines P, Rodes J. Cefotaxime is more effective than is ampicillin-tobramycin in cirrhotics with severe infections. Hepatology. 1985;5:457–462. [PubMed]
68. Chen TA, Lo GH, Lai KH, Lin WJ. Single daily amikacin versus cefotaxime in the short-course treatment of spontaneous bacterial peritonitis in cirrhotics. World J Gastroenterol. 2005;11:6823–6827. [PubMed]
69. Rimola A, Salmerón JM, Clemente G, Rodrigo L, Obrador A, Miranda ML, Guarner C, Planas R, Solá R, Vargas V. Two different dosages of cefotaxime in the treatment of spontaneous bacterial peritonitis in cirrhosis: results of a prospective, randomized, multicenter study. Hepatology. 1995;21:674–679. [PubMed]
70. Runyon BA, McHutchison JG, Antillon MR, Akriviadis EA, Montano AA. Short-course versus long-course antibiotic treatment of spontaneous bacterial peritonitis. A randomized controlled study of 100 patients. Gastroenterology. 1991;100:1737–1742. [PubMed]
71. França A, Giordano HM, Sevá-Pereira T, Soares EC. Five days of ceftriaxone to treat spontaneous bacterial peritonitis in cirrhotic patients. J Gastroenterol. 2002;37:119–122. [PubMed]
72. Angeli P, Guarda S, Fasolato S, Miola E, Craighero R, Piccolo F, Antona C, Brollo L, Franchin M, Cillo U, et al. Switch therapy with ciprofloxacin vs. intravenous ceftazidime in the treatment of spontaneous bacterial peritonitis in patients with cirrhosis: similar efficacy at lower cost. Aliment Pharmacol Ther. 2006;23:75–84. [PubMed]
73. Gómez-Jiménez J, Ribera E, Gasser I, Artaza MA, Del Valle O, Pahissa A, Martínez-Vázquez JM. Randomized trial comparing ceftriaxone with cefonicid for treatment of spontaneous bacterial peritonitis in cirrhotic patients. Antimicrob Agents Chemother. 1993;37:1587–1592. [PMC free article] [PubMed]
74. Taşkiran B, Colakoğlu O, Sözmen B, Unsal B, Aslan SL, Buyraç Z. Comparison of cefotaxime and ofloxacin in treatment of spontaneous bacterial peritonitis. Turk J Gastroenterol. 2004;15:34–38. [PubMed]
75. Navasa M, Follo A, Llovet JM, Clemente G, Vargas V, Rimola A, Marco F, Guarner C, Forné M, Planas R, et al. Randomized, comparative study of oral ofloxacin versus intravenous cefotaxime in spontaneous bacterial peritonitis. Gastroenterology. 1996;111:1011–1017. [PubMed]
76. Tuncer I, Topcu N, Durmus A, Turkdogan MK. Oral ciprofloxacin versus intravenous cefotaxime and ceftriaxone in the treatment of spontaneous bacterial peritonitis. Hepatogastroenterology. 2003;50:1426–1430. [PubMed]
77. Soares-Weiser K, Brezis M, Leibovici L. Antibiotics for spontaneous bacterial peritonitis in cirrhotics. Cochrane Database Syst Rev. 2001;50:CD002232. [PubMed]
78. Follo A, Llovet JM, Navasa M, Planas R, Forns X, Francitorra A, Rimola A, Gassull MA, Arroyo V, Rodés J. Renal impairment after spontaneous bacterial peritonitis in cirrhosis: incidence, clinical course, predictive factors and prognosis. Hepatology. 1994;20:1495–1501. [PubMed]
79. Terg R, Gadano A, Cartier M, Casciato P, Lucero R, Muñoz A, Ro mero G, Levi D, Terg G, Miguez C, et al. Serum creatinine and bilirubin predict renal failure and mortality in patients with spontaneous bacterial peritonitis: a retrospective study. Liver Int. 2008;29:415–419. [PubMed]
80. Choi CH, Ahn SH, Kim DY, Lee SK, Park JY, Chon CY, Moon YM, Han KH. Long-term clinical outcome of large volume paracentesis with intravenous albumin in patients with spontaneous bacterial peritonitis: a randomized prospective study. J Gastroenterol Hepatol. 2005;20:1215–1222. [PubMed]
81. Solà R, Andreu M, Coll S, Vila MC, Oliver MI, Arroyo V. Spontaneous bacterial peritonitis in cirrhotic patients treated using paracentesis or diuretics: results of a randomized study. Hepatology. 1995;21:340–344. [PubMed]
82. Fernández J, Monteagudo J, Bargallo X, Jiménez W, Bosch J, Arroyo V, Navasa M. A randomized unblinded pilot study comparing albumin versus hydroxyethyl starch in spontaneous bacterial peritonitis. Hepatology. 2005;42:627–634. [PubMed]
83. Sort P, Navasa M, Arroyo V, Aldeguer X, Planas R, Ruiz-del-Arbol L, Castells L, Vargas V, Soriano G, Guevara M, et al. Effect of intravenous albumin on renal impairment and mortality in patients with cirrhosis and spontaneous bacterial peritonitis. N Engl J Med. 1999;341:403–409. [PubMed]
84. Sigal SH, Stanca CM, Fernandez J, Arroyo V, Navasa M. Restricted use of albumin for spontaneous bacterial peritonitis. Gut. 2007;56:597–599. [PMC free article] [PubMed]
85. Wong F. Drug insight: the role of albumin in the management of chronic liver disease. Nat Clin Pract Gastroenterol Hepatol. 2007;4:43–51. [PubMed]
86. Garcia-Tsao G. Current management of the complications of cirrhosis and portal hypertension: variceal hemorrhage, ascites, and spontaneous bacterial peritonitis. Gastroenterology. 2001;120:726–748. [PubMed]
87. Ginés P, Rimola A, Planas R, Vargas V, Marco F, Almela M, Forné M, Miranda ML, Llach J, Salmerón JM. Norfloxacin prevents spontaneous bacterial peritonitis recurrence in cirrhosis: results of a double-blind, placebo-controlled trial. Hepatology. 1990;12:716–724. [PubMed]
88. Inadomi J, Sonnenberg A. Cost-analysis of prophylactic antibiotics in spontaneous bacterial peritonitis. Gastroenterology. 1997;113:1289–1294. [PubMed]
89. Das A. A cost analysis of long term antibiotic prophylaxis for spontaneous bacterial peritonitis in cirrhosis. Am J Gastroenterol. 1998;93:1895–1900. [PubMed]
90. Grangé JD, Roulot D, Pelletier G, Pariente EA, Denis J, Ink O, Blanc P, Richardet JP, Vinel JP, Delisle F, et al. Norfloxacin primary prophylaxis of bacterial infections in cirrhotic patients with ascites: a double-blind randomized trial. J Hepatol. 1998;29:430–436. [PubMed]
91. Novella M, Solà R, Soriano G, Andreu M, Gana J, Ortiz J, Coll S, Sàbat M, Vila MC, Guarner C, et al. Continuous versus inpatient prophylaxis of the first episode of spontaneous bacterial peritonitis with norfloxacin. Hepatology. 1997;25:532–536. [PubMed]
92. Rolachon A, Cordier L, Bacq Y, Nousbaum JB, Franza A, Paris JC, Fratte S, Bohn B, Kitmacher P, Stahl JP. Ciprofloxacin and long-term prevention of spontaneous bacterial peritonitis: results of a prospective controlled trial. Hepatology. 1995;22:1171–1174. [PubMed]
93. Dupeyron C, Mangeney N, Sedrati L, Campillo B, Fouet P, Leluan G. Rapid emergence of quinolone resistance in cirrhotic patients treated with norfloxacin to prevent spontaneous bacterial peritonitis. Antimicrob Agents Chemother. 1994;38:340–344. [PMC free article] [PubMed]
94. Esposito S, Noviello S, Leone S, Ianniello F, Ascione T, Gaeta GB. Clinical efficacy and tolerability of levofloxacin in patients with liver disease: a prospective, non comparative, observational study. J Chemother. 2006;18:33–37. [PubMed]
95. Assy N, Schlesinger S, Miron D, Hussein O. Cycling of antibiotics for the prophylaxis of recurrent spontaneous bacterial peritonitis in a cirrhotic patient. World J Gastroenterol. 2005;11:6407–6408. [PubMed]
96. Fernández J, Navasa M, Planas R, Montoliu S, Monfort D, Soriano G, Vila C, Pardo A, Quintero E, Vargas V, et al. Primary prophylaxis of spontaneous bacterial peritonitis delays hepatorenal syndrome and improves survival in cirrhosis. Gastroenterology. 2007;133:818–824. [PubMed]
97. Pauwels A, Mostefa-Kara N, Debenes B, Degoutte E, Lévy VG. Systemic antibiotic prophylaxis after gastrointestinal hemorrhage in cirrhotic patients with a high risk of infection. Hepatology. 1996;24:802–806. [PubMed]
98. Blaise M, Pateron D, Trinchet JC, Levacher S, Beaugrand M, Pourriat JL. Systemic antibiotic therapy prevents bacterial infection in cirrhotic patients with gastrointestinal hemorrhage. Hepatology. 1994;20:34–38. [PubMed]
99. Hsieh WJ, Lin HC, Hwang SJ, Hou MC, Lee FY, Chang FY, Lee SD. The effect of ciprofloxacin in the prevention of bacterial infection in patients with cirrhosis after upper gastrointestinal bleeding. Am J Gastroenterol. 1998;93:962–966. [PubMed]
100. Hou MC, Lin HC, Liu TT, Kuo BI, Lee FY, Chang FY, Lee SD. Antibiotic prophylaxis after endoscopic therapy prevents rebleeding in acute variceal hemorrhage: a randomized trial. Hepatology. 2004;39:746–753. [PubMed]

Articles from World Journal of Gastroenterology : WJG are provided here courtesy of Baishideng Publishing Group Inc
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...