Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 29  |  Issue : 2  |  Page : 454-459

Skin and soft tissue bacterial infections in cirrhotic patients with edema


1 Department of Tropical Medicine, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Dermatology and Andrology, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission14-Jan-2014
Date of Acceptance12-Apr-2014
Date of Web Publication18-Oct-2016

Correspondence Address:
Hend A Hammouda
Shebeen El-Kom, Department of Tropical Medicine, Faculty of Medicine, Menoufia University, Menoufia, 32511
Egypt
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.192421

Rights and Permissions
  Abstract 

Objective:
The aim of this study was to determine the type, risk factors, and the causative organism of bacterial skin infections in cirrhotic patients with edema.
Background:
Bacterial infections are often associated with significant morbidity and mortality in cirrhosis. The common practice of outdoor barefoot walking and the associated risk of trauma may predispose cirrhotic patients to skin infection.
Patients and methods:
This study was conducted on 150 patients, of whom 35 cirrhotic patients served as the control group. Data, including the type, the site, risk factors, and the culture results of the skin or soft tissue infection present, were collected.
Results:
A unique criterion of this study was that in all the study participants in the cirrhotic group the infection was due to posthepatitic cirrhosis (hepatitis C virus, hepatitis B virus, or combined infection). History or evidence of trauma, uncontrolled diabetes, massive lower-limb edema, and a high BMI are major risk factors for developing skin or soft tissue infection. Cellulitis represents the most common type of infection, affecting mainly the lower limbs. Gram-negative organisms are the causative organisms in cirrhotic patients (17%), mainly Escherichia coli in 13% of the cases.
Conclusion:
Gram-negative bacteria may cause bullous cellulitis in patients with cirrhosis. Trauma, diabetes mellitus, and massive lower-limb edema are major risk factors for skin and soft tissue infections in cirrhotic patients.

Keywords: cellulitis, cirrhosis, gram-negative bacteria, hepatitis, skin infections


How to cite this article:
Nouh MA, Basha MA, El-Deeb GS, Masoud BM, Hammouda HA. Skin and soft tissue bacterial infections in cirrhotic patients with edema. Menoufia Med J 2016;29:454-9

How to cite this URL:
Nouh MA, Basha MA, El-Deeb GS, Masoud BM, Hammouda HA. Skin and soft tissue bacterial infections in cirrhotic patients with edema. Menoufia Med J [serial online] 2016 [cited 2019 Nov 21];29:454-9. Available from: http://www.mmj.eg.net/text.asp?2016/29/2/454/192421


  Introduction Top


Egypt has a very high prevalence of hepatitis C virus (HCV) and a high morbidity and mortality from chronic liver disease, cirrhosis, and hepatocellular carcinoma. Approximately 20% of Egyptian blood donors are anti-HCV positive. The strong homogeneity of HCV subtypes found in Egypt (mostly 4a) suggests an epidemic spread of HCV. As a history of injection treatment has been implicated as a risk factor for HCV, a prime candidate to explain the high prevalence of HCV in Egypt is the past practice of parenteral therapy for schistosomiasis [1].

Cellulitis and erysipelas are skin infections that develop as a result of bacterial entry through breaches in the skin barrier. The incidence is about 200 cases per 100 000 patient-years [2]. Cellulitis is observed most frequently among middle-aged and elderly individuals, whereas erysipelas occurs in young children and the elderly [3],[4].

Soft tissue infections account for 11% of infections overall in cirrhotic patients and the severe form of necrotizing infection carries a high mortality rate. It is essential that clinicians make an early diagnosis and start appropriate treatment to improve outcomes of cirrhotic patients with soft tissue infections [5].

Although ∼75% of all infections in patients with cirrhosis are caused by gram-negative organisms, it is commonly assumed that skin infections are most likely caused by gram-positive organisms [6]. Staphylococcus aureus and Streptococcus pyogenes are responsible for the majority of cellulitis cases in patients without cirrhosis [7].

Gram-negative infections are considered in perianal cellulitis, immunocompromised patients [8], and patients with nephrotic syndrome [9].

Gram-negative bacteria may cause bullous cellulitis in patients with cirrhosis. Early recognition is vital, as the course of the disease is rapid, typically progressing to septic shock and death. Gram staining and culture of fluid aspirated from the bullae may aid in management [0].


  Aim of the Work Top


The aim of this work was to study skin and soft tissue bacterial infections in patients with liver cirrhosis and edema.


  Patients and Methods Top


This study was carried out in the Tropical Medicine and Dermatology Departments, Faculty of Medicine, Menoufia University Hospitals.

Participants were divided into three groups. Group I was the case group, which included 100 cirrhotic patients with skin or soft tissue bacterial infection, and was further divided into three subgroups: group Ia (10 patients classified as Child A cirrhotics), group Ib (15 patients classified as Child B cirrhotics), and group Ic (75 patients classified as Child C cirrhotics). Group II was control (a), which included 35 cirrhotic patients with edema with no skin or soft tissue infection. Group III was control (b), which included 15 patients with skin and soft tissue infection without having liver cirrhosis. After obtaining an informed consent, each patient underwent the following analyses:

  1. Detailed history taking: Personal history, patients' complaints, present history, past history of similar condition, or other diseases.
  2. Clinical examination: A thorough general and local abdominal examination was performed.
  3. Investigations: Full routine laboratory investigations included a complete blood picture, the erythrocyte sedimentation rate, the fasting serum glucose level, kidney functions (urea and creatinine), liver functions (serum protein, serum albumin, aspartate aminotransferase and alanine transaminase), and the coagulation profile (prothrombin time and concentration). Viral markers (HCV-Ab, HBs-Ag, and HIV-Ab) were determined using the enzyme-linked immunosorbent assay technique. Ascitic fluid sample analysis (total protein and albumin) and identification of bacterial growth by cultures from the skin and soft tissue infections were carried out when needed [1].
  4. Statistical analysis: Data were collected, tabulated, and statistically analyzed by a computer using SPSS version 20 (Inc., Chicago, U.S.A). Quantitative data were expressed as mean and SD (X ± SD) and analyzed by applying the F-test (one-way analysis of variance) for comparison of more than two groups of normally distributed variables and the Kruskal–Wallis test for non-normally distributed variables. Qualitative data were expressed as the number and percentage [n (%)] and analyzed by applying the c 2-test. To detect important risk factors, the logistic regression analysis was used. All these tests were used as tests of significance at P- value less than 0.05, no significance at P- value greater than 0.05, and high significance at P- value less than 0.001 [2].



  Results Top


  1. Case–control groups were well matched across demographic characteristics ([Table 1]).
  2. The present study revealed that trauma, diabetes mellitus, and a history of similar conditions were significant risk factors for developing skin and soft tissue bacterial infection ([Figure 1]).
  3. The present study revealed that cellulitis was the most common type of infection in the study population ([Table 2], [Figure 2]).
  4. In the present work, a high admission BMI represents a highly significant difference among the studied groups ([Figure 3]).
  5. The present study revealed that the period of hospitalization was significantly higher in the case group compared with the control groups ([Table 3], [Figure 4]).
  6. In the present study, there was no statistically significant difference among the studied groups regarding complications of infection ([Table 4], [Figure 5]).
  7. In the present study, there was statistically significant difference among the studied groups regarding the total gram-negative bacterial cultures ([Table 5]).
Table 1: Age and sex distribution of the studied groups

Click here to view
Table 2: Viral markers of the studied groups

Click here to view
Table 3: Length of hospitalization of the studied groups

Click here to view
Table 4: Complications of infections in the studied groups

Click here to view
Table 5: Culture results of complicated infections in the studied groups

Click here to view
Figure 1: Risk factors for developing skin or soft tissue infection. DM, diabetes mellitus

Click here to view
Figure 2: Types of skin or soft tissue infections

Click here to view
Figure 3: BMI of the studied groups

Click here to view
Figure 4: Length of hospitalization of the studied groups

Click here to view
Figure 5: Complication of skin or soft tissue infection

Click here to view



  Discussion Top


Liver cirrhosis results from a variety of mechanisms that cause progressive hepatic injury. It is the sixth leading cause of death in all patients between the ages of 35 and 55 years, and its complications continue to represent a significant worldwide healthcare burden [3].

Patients with liver diseases have an increased predisposition to infections often secondary to impaired phagocytic function, reduced complement levels, dysimmunoregulation, and corticosteroid administration. Such qualitative or quantitative impairment of humoral immunity may increase the risk of bacterial and fungal infection. Moreover, the need for invasive procedures, the use of antibacterial agents, and gastrointestinal tract bleeding associated with liver disease may result in the translocation of organisms from the gastrointestinal tract to the blood [4].

Complications of liver cirrhosis can cause severe morbidity and mortality. Bacterial infections are well-subscribed complication of cirrhosis. Patients with cirrhosis are more likely to present with community-acquired infection and to develop it during the course of hospitalization [5].

Patients with cirrhosis are extremely susceptible to bacterial infections. Although gram-negative enteric bacteria are the most commonly involved pathogens, they are not usually the etiologic agents in skin infections [6].

The mean age of group I was 55.9 ± 7.9 years, whereas that of group II was 53.9 ± 8.7 years and that of group III was 53.6 ± 8.6 years. Analysis of data obtained revealed no significant difference concerning the mean age or sex of the studied groups (P > 0.05), indicating no bias in the selection of the study population. This is consistent with all previously conducted studies concerning skin and soft tissue bacterial infection in cirrhosis [9],[17].

A unique criterion of this study was that in all the study participants in the cirrhotic groups, infection was due to posthepatitic cirrhosis: in group I, 79 patients (79%) had HCV infection, 14 patients (14%) had hepatitis B virus (HBV) infection, and seven patients (7%) had combined HCV and HBV infection, whereas in group II, 29 patients (82.9%) had HCV infection, five patients (14.3%) had HBV infection, and one patient (2.9%) had combined HCV and HBV infection. This is inconsistent with all previous studies that were based on a large number of cases with alcoholic hepatitis with cirrhosis, cardiac cirrhosis, autoimmune hepatitis, and nonalcoholic steatohepatitis [9],[17].

The present study shows that there was highly statistically significant difference between the studied groups I and II regarding the admission and the discharging BMI: the mean admission BMI of group I was 30 ± 1.7 and that of group II was 27.8 ± 2.5; the mean discharging BMI of group I was 28.8 ± 1.6 and that of group II was 24.9 ± 2.2. There was a highly statistically significant difference between studied groups I and III regarding the admission BMI: the mean admission BMI of group III was 28.3 ± 2.4. This is consistent with previous studies, which demonstrated that the admission BMI was significantly higher in cellulitis patients compared with controls [17],[18],[19].

It has been noted that the admission BMI was significantly higher in cellulitis patients compared with controls. At the time of discharge, the BMI was higher in the cellulitis group compared with control group II. This difference, however, did not reach our defined level of statistical significance. It is well known that peripheral edema is a risk factor for cellulitis. Increased edema or fluid retention results in increased patient weight. If there is an increased risk of cellulitis in cirrhotic patients, it is unclear whether this reflects the degree of edema, increased dry weight, or both [0].

Diabetes and hepatitis B and C infections were found to be significant risk factors in the study. Previous studies have identified diabetes as a risk factor [21],[22], whereas a recent case review did not [10],[23]. Our review identified HCV infection as a risk factor; a much larger case–control series comparing 34 204 HCV-infected patients with 136 816 control participants found a significantly higher incidence of cellulitis in the HCV population [4].

This study showed that the duration of hospitalization of the patients increased in the presence of skin or soft tissue bacterial infection, with the mean length of hospitalization of group I being 6.2 ± 2.9 and that of group II being 5.6 ± 2.8; there was highly statistically significant difference between the cirrhotic groups (groups I and II) regarding the length of hospitalization. This is consistent with previous studies concerning skin infection in cirrhosis [9],[17].

The present study showed that the incidence of cellulitis was more common than other types of skin and soft tissue bacterial infections in both groups (groups I and III) and provided strong evidence for an increased risk of cellulitis in cirrhotic compared with noncirrhotic patients. Furthermore, an increased risk of cellulitis was noted in complicated compared with noncomplicated cirrhosis: there were four patients(40%) in group Ia, eight patients (53.3%) in group Ib, 58 patients (77.3%) in group Ic, and seven patients (46.7%) group III. This is consistent with the study conducted by Dupuy A et al. [4].

There was no statistically significant difference between the studied groups I and III regarding complications of infection: abscess formation represents 12%, bullae and ulcer formation 11%, and severe necrotizing infection 3% in the cirrhotic group compared by 6.7% for both abscess and bullae or ulcer formation in the noncirrhotic group. This is inconsistent with a recent study by Bair MJ et al. [5] demonstrating a higher incidence of complications, mainly necrotizing fasciitis, in the cirrhotic group.

In this study, wound cultures were collected from 28 patients with complicated skin or soft tissue infection. In group I (cirrhotic group), there were 17 cultures that yielded gram-negative organisms [13 cultures positive for  Escherichia More Details coli (13%), two cultures positive for Klebsiella spp. (2%), and two cultures for Pseudomonas spp. (2%)] and there were nine cultures of gram-positive organisms [six cultures for S. aureus (6%) and three cultures for Streptococcus spp. (3%)].

In group III, (noncirrhotic group), there was no cultural growth of a gram-negative organism, and there were two cultures of gram-positive organisms [one culture for S. aureus (6.7%) and one culture for Streptococcus spp. (6.7%)].


  Conclusion Top


Diabetes mellitus, massive lower-limb edema, and trauma are major risk factors for development of skin or soft tissue infection in cirrhotic patients.

Cellulitis is the most common type of soft tissue infection in cirrhosis. Gram-negative bacteria may cause bullous cellulitis in patients with cirrhosis. Early recognition is vital, as the course of the disease is rapid, typically progressing to septic shock and death.

Most skin and soft tissue infections can be managed on an outpatient basis, although patients with evidence of rapidly progressive infection, high fever, or other signs of systemic inflammatory response should be monitored in the hospital setting.

Conflicts of interest

There are no conflicts of interest.[25]

 
  References Top

1.
Lavanchy D, McMahon B. Worldwide prevalence and prevention of hepatitis C. In: Liang TJ, Hoofnagle JH, editors. Hepatitis C. San Diego, CA: Academic Press; 2000. p. 185–202.  Back to cited text no. 1
    
2.
McNamara DR, Tleyjeh IM, Berbari EF, et al. Incidence of lower-extremity cellulitis: a population-based study in Olmsted county, Minnesota. Mayo Clin Proc 2007; 82:817-821.  Back to cited text no. 2
    
3.
Ellis Simonsen SM, van Orman ER, Hatch BE, et al. Cellulitis incidence in a defined population. Epidemiol Infect 2006; 134:293.  Back to cited text no. 3
    
4.
Eriksson B, Jorup-Rönström C, Karkkonen K, et al. Cellulitis: clinical and bacteriologic spectrum and serological aspects. Clin Infect Dis 1996; 23:1091.  Back to cited text no. 4
    
5.
Bisno AL, Stevens DL. Streptococcal infections of skin and soft tissues. N Engl J Med 1996; 334:240–245.  Back to cited text no. 5
    
6.
Holzapfel L, Jacquet-Francillon T, Rahmani J, et al. Microbiological evaluation of infected wounds of the extremities in 214 adults. J Accid Emerg Med 1999; 16:32–34.  Back to cited text no. 6
    
7.
Yoon TY, Jung SK, Chang SH. Cellulitis due to Escherichia coli in immunocompromised persons. Br J Dermatol 1998; 139:885–888.  Back to cited text no. 7
    
8.
Asmar BI, Bashour BN, Fleischmann LE. Escherichia coli cellulitis in idiopathic nephrotic syndrome. Clin Infect Dis 1987; 26:592–594.  Back to cited text no. 8
    
9.
Lipsky BA, Weigelt JA, Gupta V, Killian A, Peng MM. Skin, soft tissue, bone and joint infections in hospitalized patients: epidemiology and microbiological, clinical and economic outcomes. Infect Control Hosp Epidemiol 2007; 28:1290–1298.  Back to cited text no. 9
    
10.
Horowitz Y, Sperber AD, Almog Y. Gram-negative cellulitis complicating cirrhosis. Mayo Clin Proc 2004; 79:247–250.  Back to cited text no. 10
    
11.
Harris CCare Partners. Clinical practice policy and procedure. Semi quantitative wound swab sample culturing technique. Adv Wound Care 2000; 8:28–46.  Back to cited text no. 11
    
12.
Lind DA, Marchal WG, Wathen SA. Statistical techniques in business and economics. 12th ed. Columbus, OH: McGraw-Hill Education; 2005 6:532–620.  Back to cited text no. 12
    
13.
Mihas AA. Cirrhosis of the liver: introduction to three-article symposium. Postgrad Med 2001; 2:752–960.  Back to cited text no. 13
    
14.
Fernandez J, Navasa M, Gomez J. Bacterial infections in cirrhosis: epidemiological changes with invasive procedures and norfloxacin prophylaxis. Hepatology 2005; 35:140–148.  Back to cited text no. 14
    
15.
Navasa M, Fernandez J, Rhodes J. Bacterial infections in liver cirrhosis. Ital J Gastroenterol Hepatol 1999; 31:16–625.  Back to cited text no. 15
    
16.
Caly WR, Strauss E. A prospective study of bacterial infections in patients with cirrhosis. J Hepatol 1993; 18:353–358.  Back to cited text no. 16
    
17.
Mohan P, Ramu B, Bhaskar E, Venkataraman J. Prevalence and risk factors for bacterial skin infection and mortality in cirrhosis. Ann Hepatol 2011; 10:15–20.  Back to cited text no. 17
    
18.
Rongey C, Lim NH, Runyon BA. Cellulitis in patients with cirrhosis and edema: an under-recognized complication currently more common than spontaneous bacterial peritonitis. Open Gastroenterol J 2008; 2:24–27.  Back to cited text no. 18
    
19.
Lewis SD, Peter GS, Gómez-Marín O, Bisno AL. Risk factors for recurrent lower extremity cellulitis in a U.S. Veterans Medical Center Population. Am J Med Sci 2006; 332:304–307.  Back to cited text no. 19
    
20.
Thorsteinsdottir B, Tleyjeh IM, Baddour LM. Abdominal wall cellulitis in the morbidly obese. Scand J Infect Dis 2005; 37:605–608.  Back to cited text no. 20
    
21.
Swartz M. Cellulitis. N Engl J Med 2004; 350:904–912.  Back to cited text no. 21
    
22.
Jorup-Ronstrom C. Epidemiological, bacteriological and complicating features of erysipelas. Scand J Infect Dis 1986; 18:519–524.  Back to cited text no. 22
    
23.
Eriksson B, Jorup-Ronstrom C, Karkkonen K, Sjoblom AC, Holm SE. Erysipelas: clinical, bacteriologic spectrum and serological aspects. Clin Infect Dis 1996; 23:1091–1098.  Back to cited text no. 23
    
24.
Dupuy A, Benchikhi H, Roujeau JC, et al. Risk factors for erysipelas of the leg (cellulitis): case–control study. BMJ 1999; 318: 1591–1594.  Back to cited text no. 24
    
25.
El-Serag HB, Anand B, Richardson P, Rabeneck L. Association between hepatitis C infection and other infectious diseases: a case for targeted screening. Am J Gastroenterol 2003; 98:167–174.  Back to cited text no. 25
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Aim of the Work
Patients and Methods
Results
Discussion
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed1145    
    Printed0    
    Emailed0    
    PDF Downloaded112    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]