iMedPub Journals THE INTERNATIONAL ARABIC JOURNAL 2016

http://journals.imed.pub Vol. 6 No. 2:5

OF ANTIMICROBIAL AGENTS ISSN 2174-9094
doi: 10.3823/790

Spontaneous bacterial peritonitis Monkez M. Yousef1,

Ahmed I. Amer1, Ayaat
in the medical intensive care unit M. Zidan1, Fatma A.
Amer2, Rehab M.
of a University Hospital in Egypt: ElsaidTash2

frequency, bacteriological profile, 1Internal Medicine Department.

2Medical Microbiology and Immunology
risk factors and outcomes Department, Faculty of Medicine,
Zagazig University, Zagazig, Egypt.

Corresponding author:

Abstract Fatma A. Amer

Objective: To assess the frequency of spontaneous bacterial peritonitis  [email protected]

(SBP) in the Medical intensive care unit (ICU) of Zagazig University
Hospital, identify the causative organisms, their susceptibility to
antimicrobials, and to determine risk factors and clinical outcomes.

Methods: One hundred and eighty-nine ascitic patients suffered of

liver cirrhosis were included in this prospective study. Medical history,
physical examination, radiological reports and assessment of disease
severity were done. Diagnostic paracentesis was performed. Ascitic
fluid was subjected to chemical, hematological and bacteriological
investigations. Isolated bacteria and their antibiotic susceptibility
pattern were identified using standard methods.

Results: Frequency of SBP in ascitic patients due to liver cirrhosis

was 56.1%. Classic SBP was diagnosed in 47.2% of cases and the
remaining 52.8% were found to be culture negative neutrocytic
ascites (CNNA). Comparison of the mean standard deviation (SD)
of clinical and demographic characteristics for SBP versus non SBP
revealed significant association with hepatocellular carcinoma (HCC)
and with beta blockers(BB). Comparison between mean SD of
clinical, biochemical and microbiological characteristics for SBP variants
revealed significant association with HCC, total leucocytic count and
positive culture. Significant symptoms and signs were observed with
fever, hypotension and abdominal pain. E-coli was the most frequently
isolated bacteria (56%), followed by Klebsiella pneumoniae 24% and
Staphylococcus aureus 20%. Gentamicin was the most effective
antibiotic in- vitro against K. pneumonia and E. coli isolates, while all S.

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2016
ISSN 2174-9094 Vol. 6 No. 2:5
doi: 10.3823/790

aureus isolates were susceptible for vancomycin. Higher mortality rate

was found in patients with SBP versus those with non-SBP (p=0.024).
Predictors of mortality among patients with SBP were related to old
age and high End-Stage Liver Disease according to MELD score.

Conclusion: SBP is frequently encountered in the medical ICU as a life

threatening complication of liver cirrhosis. Early diagnosis and prompt
management guarantee improved prognosis.

Keywords: Spontaneous bacterial peritonitis, Neutrocytic ascites,

bacterial agents & antibiotic resistance

Introduction
who develop signs or symptoms suggestive of SBP.
Spontaneous bacterial peritonitis (SBP) is a com- The diagnosis of SBP is made when total white cell
mon and severe complication of cirrhotic patients count in the peritoneal fluid is greater than 500/
with ascites characterized by spontaneous infec- mm3 and polymorph nuclear leucocyte count (PMN)
tion of ascitic fluid which occurs in the absence is greater than 250/mm3. A positive bacterial culture
of any infection or perforation of intra- abdomi- of the ascitic fluid is not required for the diagnosis
nal organs [1]. Most episodes of SBP are caused of SBP [4]. When the ascitic fluid PMN are morethan
by gram-negative bacteria, but in hospital setting, 250/mm3 and the ascitic fluid culture is positive, the
gram positive-bacteria have been isolated with an case is identified as culture positive/classic SBP, if
increasing frequency in recent years. Antimicrobial the ascitic fluid PMN are more than 250/mm3 and
activity of the ascitic fluid plays very important role the ascitic fluid culture is negative, the condition
in the development of SBP [2].The clinical spectrum is identified as culture negative neutrocytic ascites
of SBP is very variable and relatively low percent- (CNNA) and when ascetic fluid PMN are less than
age of patients show the complete typical features 250/mm3 and the ascitic fluid culture is positive, the
of acute peritoneal infection with diffuse abdomi- case is diagnosed as bacterial ascites[5].Treatment of
nalpain, rebound tenderness, and reduced bowel spontaneous bacterial peritonitis has to be started
sounds. Fever is a frequent but not universal finding. immediately after diagnosis and therefore is usually
However, it may be the only clinical sign in a large empirical since culture results are not available at
proportion ofpatients. In other cases, infection is this time point. However, none of the international
manifested by hepatic encephalopathy (HE), wors- guidelines to date differentiates between nosoco-
ening of liver and/or renal function or septic shock, mial and community-acquired SBP with regard to
while the peritoneal signs maybe weak or absent. their antibiotic treatment. This may be associated
In approximately 13% of cases, SBP is asymptomatic with serious consequences since nosocomial infec-
[3]. A sample of ascitic fluid should be obtained tions are associated with high rates of multiresistant
routinely in all patients with cirrhosis and ascites ad- bacteria and mortality [6]. The efficacy and role of
mitted to hospital and in those hospitalized patients prophylactic antibiotics is highly impotant [7].

2 Received on 8 July 2016; Accepted on 11 October 2016 This article is available from: www.iajaa.org / www.medbrary.com
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2016
ISSN 2174-9094 Vol. 6 No. 2:5
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Epidemiological studies about SBP in medical ICUs severity was assessed using Child Pugh score and
in Sharkia Governorate are scarce. To the best of our modified Child-Pugh classification of severity of liver
knowledge there is no study about the magnitude disease [8], and MELD score. Paracentesis was car-
of this problem in our hospital. Therefore, this study ried out using a 23-gauge sterile needle under local
has been done to assess the frequency of SBP and anesthesia with lidocaine. Ascitic fluid samples were
its variants in the Medical ICU of Zagazig University collected under complete aseptic technique. Ten ml
Hospital, to identify the causative bacterial flora and of the fluid was inoculated immediately into aerobic
their susceptibility profile to antimicrobials, and to and anaerobic blood culture bottles (Oxoid, Signal
determine risk factors for acquisition of this clini- Blood Culture System)) at the bedside. Two ml of
cal condition. Another objective was to assess the blood was added to an EDTA vacutainers (Tradekey,
clinical outcomes; and to determine their predictors. Egypt) to test for gross appearance, cell counts and
differential count and two ml were added to a hep-
Patients and Methods arinized tube for chemistry testing [9].Subcultures
of the blood culture bottles were made on blood
A total of 189 patients hospitalized in the medi- agar and MacConkeysagar (Oxoid Basingstoke, UK)
cal ICU of the Internal Medicine Department of Za- and were incubated aerobically and anaerobically
gazig University Hospital were enrolled in this cross at 37C for 24 hours. Growing colonies were iden-
sectional study. tified by conventional microbiologic tests, and by
This hospital is a university-affiliated and located API 20 E (Bio-Merieux, France) for gram negative
in Zagazig city; the capital of Sharkya Governorate aerobic bacilli. All isolated strains were tested for an-
in the eastern province of Egypt. timicrobial sensitivity test by standardized disk diffu-
Informed written consent was obtained from sion technique [10]. The following antibiotics were
each enrolled case, and approval for conducting the used: amikacin 30 ug, amoxicillin/clavulinate 20/10
study was obtained from the Institutional Review ug, ampicillin/sulbactam 10/10 ug, azteronam 30
Board, Zagazig Faculty of Medicine. Inclusion criteria ug, cefepime 30 ug, cefotaxime 30 ug,ceftazidime
included diagnosis of ascites with complicating liver 30 ug, ceftriaxone 30 ug, cefuroxime 30 ug, gen-
cirrhosis, and age of 18 years. Exclusion criteria tamycin 10 ug, imipenem10 ug and meropenem 10
included antibiotic use in the previous two weeks, ug.
failure to obtain ascitic fluid specimen, refusal of pa- Statistical Analysis: Data were collected, en-
tients to participate in the study and incomplete pa- tered and checked to SPSS program version 17.
tients data (biochemical, clinical). A complete medi- Data were expressed as mean standard deviation
cal history was collected from each patient. Data in quantitative variables, number and percentage
included personal history, signs and symptoms (fe- for qualitative variables.Categorical data were com-
ver, abdominal pain, GIT bleeding, HE), medications pared using the chi-square test or fishers exact test
(proton pump inhibitors PPI and beta- blockers in and are expressed as percentage. Statistical signifi-
the previous two weeks), and underlying diseases cance was defined as P less than 0.05. Continuous
(e. g., diabetes, mellitus, ischemic heart disease, covariates that were not normally distributed were
chronic obstructivepulmonary disease and renal categorized using standard quartiles.The logistic
disorders). All the patient were subjected to thor- regression model was used to perform both the
ough physical examination with emphasize being univariate and multivariate analysis to examine as-
placed on abdominal examination, routine labora- sociations between outcomes and clinical and bio-
tory investigations and radiological studies. Disease chemical variable.

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2016
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doi: 10.3823/790

Results Table I. Clinical and demographic characteristics

and outcomes of study population
A total of 189 patients were the subject of this Characteristics
Total patients
No=189
study, 118 were males and 71 were females. Their
ages ranged from 30- 94 years, and 67 were smok- Sex
Male: N (%) 118(62.4)
ers. MELD score ranged from 6- 54, and 102 had Female: N (%) 71 (37.6)
associated infection. Random blood glucose level
Age(years) mean SD (range) 60.313 (30-94)
(mean SD) was 184.5 105 (Table 1). All other
Smokers: N (%) 67 (35.4)
Risk factors, signs and symptoms and biochemi-
cal and hematological analysis of ascitic fluid are MELD score mean SD (range) 21.39.7(6-54)

shown in Table 1. Out of the 189 patients with Associated infection: N (%) 102 (54)
ascites due to liver cirrhosis, 106 were diagnosed Random blood glucose(mg/dl) 184.5105
as SBP; 50 were classic SBP and 56 were CNNA. mean SD

Biological characteristics of ascitic fluid samples in Risk factors:

HCC: N (%) 71(36.6 )
patients with SBP and number and type of each PPI: N (%) 12(6.3 )
bacterial isolates are shown in Table 2. Gentamicin BB: N (%) 41(21.7 )
was the most effective antibiotic in- vitro against Diabetes: N (%) 67(35.4 )

K. pneumonia and E. coli, while S. aureus. was Signs and symptoms:

Fever: N (%) 88(46.6 )
100% susceptible to vancomycin. The susceptibility Abdominal pain: N (%) 78(41.3 )
of tested antibiotics is shown in Table 3. When the GI bleeding: N (%) 23(12.2 )
HE: N (%) 42(22.2 )
mean SD of clinical and demographic character- Hypotension at presentation: N (%) 31(16.4 )
istics for SBP and non-SBPwere compared, 36.6%
Biochemical and hematological
of patients had hepatocellular carcinoma; 63.6% of analysis of ascitic fluid:
them were having SBP and 32.4% were negative. Total leucocytic count (Cells\l): 925.81232(100-8000)
mean SD (range)
Beta blockers were used by 21.7% of study group, Neutrophile cells\l: (median- range) 170(25-2200)
mainly by those diagnosed to have non SBP. Patients Total protein g\dl (median- range) 1320(71-8800)
Glucose (mg\dl): mean SD 174.7113
with SBP were more likely to presentwith fever than LDH(IU\l): median-range (Range) 110(30-914)
those withnon SBP, whereas the latter group of
Child-Pugh score: mean SD (range) 9.72.3(7-15)
patients were morelikely to present with hypoten-
Prothrombin time(seconds): 18.16.7
sion than the former group. The rest of compared mean SD
variableare shown in Table 4. Comparison between
Pro Time INR (mean SD) 1.50.6
characteristics of SBP variants showed that mortality
Mortality: N (%) 52(27.5 )
is higher in patients with SBP versus non-SBP. No
statisticallysignificant difference occurred between ICU stay(days):meanSD(Range) 5.41.8(3-9)

SBP and non-SBP regarding ICU stay. The univari- Abbreviations; MELD: Model for End stage Liver Disease, PPI:
proton pump inhibitor, HCC: hepatocellular carcinoma, BB: beta
ate analysis for risk factors for mortality among SBP blocker, GI: gastro-intestinal, HE: hepatic encephalopathy
patients revealed thatage andMELDscore were the
only significant factors for mortality (p 0.001 and
p0.003, respectively). When the two variables were
introduced into a multivariate regressionmodel, they
remained as independent risk factor for mortality biochemical and microbiological characteristics for
(Table 4). Comparison of most important clinical, SBP variants is shown in Table 5.

4 Received on 8 July 2016; Accepted on 11 October 2016 This article is available from: www.iajaa.org / www.medbrary.com
 THE INTERNATIONAL ARABIC JOURNAL OF ANTIMICROBIAL AGENTS
2016
ISSN 2174-9094 Vol. 6 No. 2:5
doi: 10.3823/790

Table 2. B
 iological characteristics of ascitic fluid in Cases of SBP encountered in this work where
patients with SBP either the classical or CNNA type, which goes in
SBP No=106
accord with the findings of Iqbal et al [11]. Our rates
Characteristics
mean SD of the classical and the CNNA types are also com-
Total leucocytic count in ascitic
parable to those estimated by Amjad et al. (13),
sample (cells\l): median-range 900 (500-8000) and Nepal et al. (14). Concerning bacterascitis type;
Neutrophil count (cells\l):
whereas no cases were diagnosed during the cur-
median-range 450(250-2200) rent work, it has been stated to range between
Total protein (mg\dl): median-range 1381(71-8800)
3.7% and 11.1% in other studies (13- 14). Differ-
ences in the occurrence of bacterascitic cases may
Glucose (mg\dl): mean SD 176120
be due to differences in the severity of the under-
LDH (IU\l): median-range 111(30-914) lying liver disease or in timing of paracentesis or
Causative bacteria isolates culture methods.
E. coli: N (%) 28 (56 ) Investigations are required for accurate diagno-
Klebsiella: N (%) 12 (24 )
Staph. aureus: N (%) 10 (20 ) sis. The first step is diagnostic paracentesis. Ascitic
fluid culture is also needed to identify the causative
agents.
Dissimilar to secondary peritonitis, SBP are usu-
Discussion ally monomicrobic [15]. The predominance of gram-
negative bacteria in our work coincides with other
Spontaneous bacterial peritonitis (SBP) is one of reports [16]. These results support the theory of bac-
the most common and life-threatening problems terial translocation as the most probable mechanism
of liver cirrhosis. The frequency of SBP in patients responsible for the occurrence of SBP in cirrhotic
admitted to our Medical ICU with ascites and com- ascitic patients. Translocation of intestinal bacteria
plicating liver cirrhosis is 56.1% . Remarkably, this is somewhat organism-specific; gram-negative bac-
rate is higher than rates from other parts of the teria translocate more efficiently than gram-positive
world [1, 11, 12]. bacteria or anaerobes [17].

Table 3. Antibiotic susceptibility of the isolated bacteria

Bacteria
N (%) Susceptible to:
(N ) tested

AMP/
AMK CFZ CTX CIP ERY GEN MEM OXA PEN TZP RIF TMP VAN
SAM
E. coli (28) 4 9 5 8 0 0 14 3 0 0 8 0 4 0
(14) (32) (18) (28) (0 ) (0 ) (50 ) (11) (0 ) (0 ) (29 ) (0 ) (14 ) (0 )

Klebsiella 7 4 8 0 0 12 2 0 0 4 0 2 0
(12) 3 (25)
(58) (33) (67) (0 ) (0 ) (100 ) (17) (0 ) (0 ) (33) (0 ) (17) (0 )

S. aureus 5 2 4 9 9 3 1 10 3 10 5 3 10
(10) 1 (10)
(50) (20) (40 ) (90 ) (90 ) (30 ) (10 ) (100 ) (30 ) (100) (50 ) (30 ) (10 )

AMK: Amikacin; Ampicillin+ sulbactam: AMP/SAM; Cefazolin: CFZ; Cefotaxime: CTX; Ciprofloxacin ; CIP; Clindamycin: CLI; Erythromycin:
ERY; Gentamycin: GEN; Imipinem: IPM; Meropnem: MEM; Oxacillin: OXA; Penicillin: PEN; Piperacillin/tazobactam: TZP; Rifampicin: RIF;
Trimethoprim: TMP; Vancomycin: VAN.

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Table 4. Comparison of clinical and demographic characteristics for SBP and non SBP

SBP Non SBP

Characteristics Significance
No=106 No=83

Age(years):meanSD (Range) 61.514.5(30-94) 58.710.7(36-89) 0.13*

Male: N (%) 64 (54.2) 54 (45.8)
Female: N (%) 42(59.2) 29 (40.8) 0.5**
Smokers: N (%) 35(52.2) 32(47.8) 0.47**
MELDscore:meanSD (Range) 21.89.2(8-45) 20.610.3(6-54) 0.38*
Associated infection: N (%) 51(58.6) 36(41.4) 0.51**
Random blood glucose (mg\dl):meanSD 193.5114 172.892 0.1*
Risk factors: N (%)
HCC 48(63.6) 23(32.4 ) 0.013**
PPI 6(50) 6(50 ) 0.66**
BB 15(36.6 ) 26(63.4 ) 0.004**
Diabetes 35(52.2 ) 32(47.8 ) 0.42**
Complaint: N (%)
Fever: 61(69.3 ) 27(30.7 ) 0.001**
Abdominal pain 48(61.5) 30(38.5) 0.2**
G I bleeding 9(39.1) 14(6.09) 0.08**
H.E. 21(50) 21(50) 0.36**
Hypotension at presentation: N (%) 10(32.3 ) 21(67.7) 0.003**
Child-pugh score: meanSD(Range) 9.62.3(7-15) 9.72.3(7-15) 0.64*
Prothrombin time(seconds):meanSD 18.17.6 17.15.1 0.09*
INR: meanSD 1.40.6 1.50.5 0.42**
Abbreviations; MELD: Model for End stage Liver Disease, PPI: proton pump inhibitor, HCC: hepatocellular carcinoma, BB: beta blocker, GI:
gastro-intestinal, HE: hepatic encephalopathy, Level of significance calculated b *: t- test **: X2test

However, it is to be emphasized that the etiology Reputable organizations have recommended

of gram positive cocci in SBP has markedly increased several antibiotics that might be used for empirical
recently.Streptococci (mostly pneumococci), have treatment in community based SBP. In a nosoco-
been found to be common organisms in patients mial setting patient should receive empiric antibi-
who are not receiving selective intestinal decon- otic therapy according to the local susceptibility of
tamination [18]. S. aureus is an emergent bacteria bacteria. This is of particular concern due to recent
in patients who have been treated with antibiotic changes in the microbial flora of SBP, and increased
prophylaxis (quinolones) and/or underwent invasive incidence of antibiotic- resistant gram-negative bac-
procedures [19-20]. S. aureus accounted for 20% teria mostly due to the widespread usage of qui-
of isolated organisms in the present work, which is nolones for prophylaxis. With appropriate antibiotic
comparable to other studies [19], but is less than treatment of SBP, infection-related mortality can ap-
report given by Fernandez et al., [20]. No obligate proach zero [22].
anaerobes were isolated as in other studies. The Hepatocellular carcinoma was identified as a risk
reduced capability of intestinal anaerobes for trans- factor; an anticipated issue due to the negative ef-
location and the relatively high oxygen content of fect of HCC on the immune system.
ascitic fluid are considered inhibiting factors [21]. We found no relation between prior use of

6 Received on 8 July 2016; Accepted on 11 October 2016 This article is available from: www.iajaa.org / www.medbrary.com
 THE INTERNATIONAL ARABIC JOURNAL OF ANTIMICROBIAL AGENTS
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Table 5. Comparison of clinical and demographic characteristics for SBP variants

Classic SBP CNNA
Characteristics Significance
No=50 No=56
Age(years):meanSD 61.714 61.415.2 0.91*
Male: N (%) 31(62) 33(58.9)
0.74**
Female: N (%) 19(38) 23(41.1)
Smoking: N (%) 19(38) 40(71.4) 0.3**
Risk factors: N (%)
HCC 15(30) 33(58.9) 0.002**
PPI 5(10) 1(1.8) 0.15**
BB 9(18) 6(10.7) 0.28**
Diabetes 17(34) 18(32.1) 0.83**
Child-pugh score: meanSD 9.52.2 9.62.3 0.81*
Complaint: N (%)
Fever 19(38.0 ) 42(75) 0.001**
Abd. Pain 9(18.0 ) 39(69.6 ) 0.001**
G I bleeding 4(8 ) 5(8.9 ) 0.85**
HE 13(26) 8(14.3 ) 0.13**
Hypotension at presentation 6(12) 4(7.1 ) 0.6**
Associated infections: N (%) 23(46.0%) 28(50) 0.67**
Random blood sugar(mg/dl):meanSD 188.9113. 197.7115.2 0.69*
Total protein(g/dl):meanSD 1695.51081 16081321 0.71*
Total leucocytic count(cells/l):meanSD 1136667 1767.31814 0.02*
Prothrombin time(seconds):meanSD 17.95.7 19.59.0 0.29*
INR: meanSD 1.520.7 1.360.5 0.19*
LDH(IU/l):meanSD 211.2161. 159.0164.1 0.1*
Glucose(mg/dl):meanSD 192153 197.7115.2 0.69*
Neutrophilcount(cells/l):meanSD 865.7527 897.4813.7 0.815*
Abbreviations; MELD: Model for End stage Liver Disease, PPI: proton pump inhibitor, HCC: hepatocellular carcinoma, BB: beta blocker, GI:
gastro-intestinal, HE: hepatic encephalopathy
Level of significance calculated by
*: t- test, **: X2test

proton pump inhibitor (PPI) and SBP as reported These contradictory conclusions require more inves-
by similar studies [23]. Additionally, patients using tigations before BBS use can be endorsed for the
Beta blockers (BBS) were less liable to develop SBP; routine management of ascites.
however such medication had nothing to do as a Fever and hypotension were significantly asso-
differentiating factor for presenting with a specific ciated with diagnosis of SBP among our patients.
SBP variant. BBS prevent variceal bleeding through Contrary to earlier studies, abdominal pain was a
decreasing portal pressure which is theoretically symptom significantly associated with the CNNA.
supposed to benefit patients. Reducing portal hy- Total leukocytic count is significantly higher in CNNA
pertension may decrease intestinal translocation of than classic type. This result could lead to better
microorganisms into the peritoneal cavity [25]. In ability of ascetic fluid to remove bacteria leading
contrast, other studies have identified Beta blockers to the CNNA variant, a finding that needs further
use as an independent risk factor for death [26]. studies.

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8 Received on 8 July 2016; Accepted on 11 October 2016 This article is available from: www.iajaa.org / www.medbrary.com
 THE INTERNATIONAL ARABIC JOURNAL OF ANTIMICROBIAL AGENTS
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treated with beta;-blockers. Am J Gastroenterol 2012;107:418- Comment on this article:

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