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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 29  |  Issue : 4  |  Page : 846-854

Study of bacteremia in diabetic patients


1 Department of Medical Microbiology and Immunology, National Liver Institute, Menoufia, Egypt
2 Department of Medical Microbiology and Immunology, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission15-Aug-2015
Date of Acceptance20-Oct-2015
Date of Web Publication21-Mar-2017

Correspondence Address:
Eman H Hassan Salem
Shebien El Kom, Menoufia, 32511
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.202512

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  Abstract 

Objectives
The objective of this study was to assess the rate of bacteremia, the most common bacteria, its antibiotic sensitivity pattern, and the role of immunity in its occurrence in diabetic patients.
Background
Bacteremia constitutes the most severe end of the spectrum of frequent community-acquired infections, and the prevalence, and thus disease burden, of bacteremia has increased during the past decades analogous with diabetes.
Materials and methods
A total of 160 individuals (93 male and 67 female with a mean age of 48.0 ± 9.7 years) were divided into the following groups: 60 diabetics with infections (group I), 70 nondiabetics with infections (group II), and 30 apparently healthy persons as controls; the studied groups were subjected to full medical history, clinical examination, and bacteriological examination of blood, antibiotic sensitivity pattern for the isolated microorganisms, measurement of serum IgM, IgG by radioimmunodiffusion, and T lymphocyte level by flow cytometry.
Results
The rate of bacteremia in group I was significantly higher than in group II (P = 0.007), the level of IgM and CD3 in group I was significantly higher than in group II (P = 0.003), and total leucocytic count in group I was significantly higher than in group II (P < 0.001). Staphylococcus aureus was the most common organism isolated form blood of diabetic patients, and 90.9% of them were sensitive to amikacin, followed by imipenem, vancomycin, and ceftriaxone (81.8%).
Conclusion
Diabetes increases the risk of exposure to bacteremia and affects the immune response to bacteremia.

Keywords: bacteremia, CD3, diabetes mellitus, IgG, IgM


How to cite this article:
Ghonim EM, El Hindawy GR, Abd El Motelb TM, Labib AZ, Ahmady I, Hassan Salem EH. Study of bacteremia in diabetic patients. Menoufia Med J 2016;29:846-54

How to cite this URL:
Ghonim EM, El Hindawy GR, Abd El Motelb TM, Labib AZ, Ahmady I, Hassan Salem EH. Study of bacteremia in diabetic patients. Menoufia Med J [serial online] 2016 [cited 2020 Feb 26];29:846-54. Available from: http://www.mmj.eg.net/text.asp?2016/29/4/846/202512


  Introduction Top


Bacteremia is a clinical entity associated with the presence of viable bacteria in the bloodstream, as evidenced by blood cultures in which contamination has been effectively ruled out [1].

Bacteremia is associated with high morbidity and mortality. Despite the availability of effective antibiotics and improved treatment of circulatory failure and organ dysfunctions, the 30-day mortality from bacteremia still averages 20%. Mortality may be even higher in older patients with coexisting chronic diseases. Prompt detection and treatment is therefore an important goal for improving patient prognosis [2].

Diabetes mellitus (DM) is a group of metabolic diseases characterized by hyperglycemia with disturbances of carbohydrate, fat, and protein metabolism, resulting from defects in insulin secretion, insulin action, or both. The chronic hyperglycemia of diabetes is associated with long-term damage, dysfunction, and failure of various organs, especially the eyes, kidneys, nerves, heart, and blood vessels [3].

Chronically ill and immunocompromised patients with DM have an increased risk of bacteremia [4]. On the other hand, their antimicrobial function is inhibited by hyperglycemia because of the inhibition of glucose phosphate dehydrogenase [5]. In addition, there is an increase in adherence of microorganisms and they grow better in glucose; in addition to impaired host defense mechanisms such as impaired granulocyte function, decreased cellular immunity, impaired complement function, and decreased lymphokine response may be influenced by glycemic control [5].


  Materials and Methods Top


The study was carried out during the period from November 2013 to July 2014 at Menofiya University Hospital and Sheben-elkom Teaching Hospital; it was conducted on 160 individuals (93 male and 67 female with a mean age of 48.0 ± 9.7 years) who were classified into the following groups – group I: 60 diabetic patients with infections, group II: 70 nondiabetic patients with infections, and group III: 30 apparently healthy persons matched for age and sex as a control group.

The study was approved by the research medical ethics committee of Menoufia University Hospital, and all patients gave their written informed consent before the study.

The studied individuals were subjected to the following:

  • Full history taking and complete clinical examination
  • Blood sample collection:
    • Twenty milliliters of blood was collected for both aerobic and anaerobic culture
    • Five milliliters of blood was collected for quantitative determination of serum level of IgM and IgG: using radioimmunodiffusion
    • Five milliliters of blood was collected on EDTA for CD3 percent assessment using flow cytometry.


Methods

  • Blood culture:
    • About 20 ml of venous blood was collected from each subject under complete aseptic conditions and divided into both aerobic and anaerobic biphasic blood culture bottles, incubated at 35–37°C, and examined daily for up to 14 days for bacterial growth [6]
    • All colonies grown on agar of blood culture bottles were subjected to direct Gram staining and subcultured onto nutrient agar, blood agar, mannitol salt agar, MacConkey agar, and Sabouraud's dextrose agar, and incubated at 37°C under aerobic and anaerobic conditions for 24 h
    • Identification of aerobic and facultative anaerobes was done according to standard microbiological methods
    • Identification of anaerobic bacteria was done by Vitek 2 compact [7]
  • Antibiotic sensitivity of isolated aerobic and facultative anaerobes:
    • Antimicrobial susceptibility was determined by disc diffusion method and interpreted according to CLSI [8]
  • Quantitative determination of serum level of IgM and IgG:


This was done by use of Diffu-Plate kits (Biocientífica S.A., Argentina) [9].

Method principle

The procedure depended on immunoprecipitation in agarose and was performed by incorporation of antibody into a layer of agarose gel, and then by introduction of the antigen into wells, duly punched in the gel. The antigen was diffused radially out of the well in the surrounding gel–antibody mixture to form a visible ring of immunoprecipitation by their reaction; the diameter of the ring was directly proportional to the concentration of antigen and was expressed by linear ratio, and evaluation occurred using a reference table (end-point method):

CD3 percent measurement was done using flow cytometry assessment of (BD Simultest CD3 Reagent (Benex Limited, Dublin, Ireland)) [10].

Principles of the procedure

When monoclonal antibody reagents were added to human whole blood, the fluorochrome-labeled antibodies bound specifically to antigens on the surface of leukocytes. Monoclonal antibodies were used to identify lymphocyte subpopulation.

An aliquot of the stained patient sample was introduced into the flow cytometer and passed in narrow stream through the path of a laser beam. The stained cells fluoresce when excited by the laser beam, and the emitted light was collected and processed by the flow cytometer.

Statistics

Quantitative data were statistically described in terms of range, mean, SD, frequencies, and relative frequencies when appropriate. Comparison of quantitative variables between the study groups was done using t- test for paired samples. A probability value (P value) less than 0.05 was considered statistically significant. All statistical calculations were performed using computer package SPSS Inc. Released 2007. SPSS for Windows, Version 16.0. (SPSS Inc., Chicago, USA) [11].


  Results Top


In this study, we found that there was no significant statistical difference between the studied groups as regards age and sex ([Table 1]).
Table 1 Demographic data among the studied groups

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The incidence of bacteremia in group I was 66.7%, whereas the incidence of bacteremia in group II was 43.9%, with a highly significant difference between the two groups ([Table 2]).
Table 2 Incidence of bacteremia in the studied patients

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Fifty-five percent of organisms isolated from blood culture of diabetic patients were Gram-positive organisms (50% of them were Staphylococcus aureus), whereas 40% were Gram-negative organisms (15% were  Escherichia More Details coli) and 5% were anaerobes (50% were Bacteroid fragilis and 50% were Clostridium perfringens), and thus the most common organism isolated from group I was S. aureus, 27.5% [Table 3] and [Figure 1].
Table 3 Isolated organisms from blood culture of the studied patients

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Figure 1: Isolated organisms from blood culture of the studied patients.

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For S. aureus isolated from diabetic patients, it was highly sensitive to amikacin (90.9%) and then to each of imipenem, ceftriaxone, and vancomycin (81.8%), whereas it was highly resistant to piperacillin (81.8%) and then to amoxycillin–clavulinic acid (72.7%) [Figure 2].
Figure 2: Antibiotic sensitivity of Staphylococcus aureus in group I.

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The incidence of bacteremia in type I and type II diabetic patients was 60 and 70%, respectively, with no significant difference between them [Figure 3].
Figure 3: Relation of type of diabetes and occurrence of bacteremia in group I.

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The occurrence of bacteremia in diabetic patients was highly significantly increased with urinary tract infection (UTI) (100%) and pneumonia (100%), whereas 87.5% of endocarditis cases were associated with bacteremia with a significant increase ([Table 4]).
Table 4 Relation between type of infection and occurrence of bacteremia in group I

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Regarding immunological factor, we found a significant increase in IgM level in group I (312.82 ± 46.2) compared with group II (287.1 ± 50.99).

However, there was a nonsignificant increase in IgG level in group I (2068.6 ± 306.0) compared with group II (2163.3 ± 360.8).

With regard to CD3 level, our study showed that there was a significant increase in CD3 level in group I (62.53 ± 14.35) compared with group II (54.5 ± 15.7).

Finally, we found that there was a highly significant increase in TLC level in group I (25.2 ± 7.04) compared with group II (15.8 ± 3.3) ([Table 5]).
Table 5 Immune response (IgM, IgG, CD3, and TLC) levels among the studied groups

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There was a significant increase in the levels of IgM, CD3, and TLC in bacteremic diabetic patients than nonbacteremic diabetic patients, whereas there was no significant difference between bacteremic diabetic patients and nonbacteremic diabetic patients as regards IgG level [Figure 4].
Figure 4: Relation between bacteremia and immune response (IgM, IgG, CD3, and TLC) in diabetic patients.

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There was a highly significant increase in the level of IgG and TLC in diabetic patients with bacteremia compared with nondiabetic patients with bacteremia, whereas there was no significant difference between bacteremic diabetic patients and bacteremic nondiabetic patients as regards IgM and CD3 levels [Figure 5].
Figure 5: Relation of diabetes and immune response (IgM, IgG, CD3, and TLC) in bacteremic patients.

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The receiver operating characteristic (ROC) curve showed that with regard to IgM level in diabetic patients, at a cutoff point of 294.95, the sensitivity was 82.5%, specificity was 60%, and accuracy was 75%. However, it had a significant role in the diagnosis of bacteremia in diabetic patients. We also found that at a cutoff point of 1905.45 the sensitivity of IgG for diagnosis of bacteremia in diabetic patients was 75%, specificity was 40%, and its accuracy was 63.3%. For CD3 level, the sensitivity for diagnosis of bacteremia in diabetic patients was 75%, specificity was 55%, and its accuracy was 68.3% at a cutoff point of 56.5 [Figure 6].
Figure 6: Receiver operating characteristic (ROC) curve to diagnose bacteremia among infected diabetes patients.

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  Discussion Top


Bacteremia is usually defined as the presence of viable bacteria in the bloodstream, as evidenced by blood cultures. Bacteremia was responsible for the high increase in the mortality rate in old patients with coexisting chronic diseases. Bacteremia was ranked the 10th leading cause of death constituting the largest group of severe infections with known microbial etiology, especially pneumonia and UTI [12].

DM describes a metabolic disorder of multiple etiology characterized by chronic hyperglycemia with disturbances of carbohydrate, fat, and protein metabolism resulting from defects in insulin secretion, insulin action, or both. The effects of DM include long-term damage, dysfunction, and failure of various organs [13].

DM is the fifth most common cause of death in the world, and it is estimated that one in eight deaths (12.2%) among 20 to 79-year-olds were attributable to this condition in 2010 [14].

Several factors could predispose diabetic patients to infections including bacteremia. These factors include genetic susceptibility to infection; altered cellular and humoral immune defense mechanisms; local factors including poor blood supply and nerve damage; and alterations in metabolism associated with diabetes. Chronically ill and immunocompromised patients with DM have an increased risk of bacteremia. They may also develop bacteremia and fungemia [5].

In this study, we aimed to asses the rate of bacteremia in diabetic patients, and to know the most common bacteria causing bacteremia in diabetic patients and its antibiotic sensitivity pattern, as well as to assess the role of both types of immunity, cell mediated (T lymphocyte) and humoral (IgM, IgG), in the occurrence of bacteremia in diabetic patients.

We found that there was a highly significant increase in the incidence of bacteremia in diabetic patients (66.7%) compared with nondiabetic patients (42.9%).

This is in agreement with the study of Thomsen et al. [15], who found that the occurrence of bacteremia in diabetic patients was 68%, but in nondiabetic patients it was 59%. In addition, Wiese et al. [16] found that a rate of reinfection associated with bacteremia is two-fold higher among diabetic patients compared with nondiabetic patients.

On the other hand, Burekovic et al. [17] found that the incidence of generalized bacteremia and sepsis in diabetic patients with infection represented 6.9%. In addition, Peralta et al. [18] found that 16.3% of diabetic patients only were complicated into bacteremia.

This result may be explained by the difference in healthcare measures between the advanced and the developing countries, thus decreasing the complications of diabetes including bacteremia because of proper control of diabetes or because of proper measures of infection control [14].

However, Landrum et al. [19] found that the annual incidence rates for hospital-onset bacteremia in nondiabetic patients decreased from 0.7 per 100 000 person-years in 2005 to 0.4 per 100 000 person-years in 2010.

We also found that the incidence of bacteremia in type I diabetic patients and type II diabetic patients was 60 and 70%, respectively.

The same results were obtained by Burekovic et al. [17], who found that the incidence of bacteremia in type I diabetic patients and type II diabetic patients was 38 and 45.3%, respectively, as well as by Al-Saadi et al. [20], who found that the incidence of bacteremia in type I diabetic patients was 28.57% and its incidence was 22.2% in type II diabetic patients.

On the other hand, Thomsen et al. [15] found that enterobacterial bacteremia in diabetic patients mostly with DM type 1 had a 15-fold increased risk compared with type 2 DM patients.

These results may be explained by the principle that the ability of exposure to different types of infections in diabetic patients including bacteremia depends on the status of the immune system of the diabetic patients, their glycemic control during the period of diabetic illness, and the effect of DM on their different organs, not on the type of diabetes [14].

We found that 55% of organisms isolated from blood culture of diabetic patients were Gram-positive organisms (50% of them were S. aureus), whereas 40% were Gram-negative organisms (15% were E. coli) and 5% were anaerobes (50% were B. fragilis and 50% were C. perfringens); therefore, the most common organism isolated from group I was S. aureus, 27.5%.

This result is in agreement with that of Prakash et al. [21], who found that from the total isolated bacteria from blood of the patients 57.8% were Gram positive [Streptococcus spp. (21.1%), coagulase-negative Staphylococci (20.8%), and S. aureus (11.4%)], whereas Gram-negative bacteria represented 42.2% [E. coli (11.9%), Klebsiella pneumoniae (2.5%), Pseudomonas aeruginosa (3.1%), and Proteus spp. (3.1%)]. In addition, in the study by Ahmed et al. [22], the result of analysis of organisms causing bloodstream infection in Assiut in Egypt revealed that 69.1% of the organisms were Gram positive, and S. aureus was the most commonly isolated organism (18.9%), and Gram-negative organisms represented 29.1%, where K. pneumoniae was the most common (10.3%) organism followed E. coli (8.6%).

On the other hand, Revelas and Stefanidis [23] found that E. coli is the cause of 80–85% of UTIs, complicated with bacteremia followed by Staphylococcus saprophyticus, which was the cause in 5–10% of these cases. Our results were nearly similar to the results detected by Al-Saadi et al. [20], who found that Gram-positive organisms represented 70% of organisms causing bacteremia in diabetic patients, in which Staphylococcus epidermidis was the most common one (61.9%). In addition, Mahmood [24] found that S. aureus represented 39.5% of aerobic organisms isolated from bacteremia.

On the other hand, Thomsen et al. [15] found that the most common isolated organism in patients with enterobacterial bacteremia was E. coli – 83% in diabetic patients and 80% in nondiabetic patients – followed by Klebsiella spp. –9% in diabetic patients and 12% in nondiabetic patients. In addition, Peralta et al. [18] concerning diabetic patients and Retamar et al. [25]concerning nondiabetic patients found that E. coli was the most common organism isolated from patients with enterobacterial bacteremia –77.5 and 36%, respectively. However, VonEiff et al. [26] mentioned that Klebsiella spp. represented 44.4% of all Gram-negative bacteria isolated from blood of diabetic patients.

We found that the occurrence of bacteremia was highly significantly increased with UTI (100%) and pneumonia (100%), whereas 87.5% of endocarditis cases were associated with bacteremia, with a significant increase.

Similarly, Thomsen et al. [15] reported that 100% of diabetic patients with UTI infections were complicated by bacteremia. Zubair et al. [27] and Bhat et al. [28] found that among diabetic patients admitted to hospital with diabetic foot infection, 87.5% were complicated with bacteremia.

On the other hand, Pogorzelska-Maziarz et al. [29] found that S. aureus bacteremia usually complicates renal failure (85%) followed by cirrhosis, and central venous catheter (62.7%). Babay [30] found that the major source of bloodstream infection with bacteria was prolonged stay in ICU and intervenous catheterization due to infection with endocarditis (17.1%), followed by pneumonia (14.6%), liver abscess (7.3%), and UTI (6.1%). Wiese et al. [16] found that S. aureus bacteremia is two-fold higher among patients with UTI (90%) because of frequent exposure to the procedure of dialysis followed by liver abscess (58%).

Regarding immunological factor, we found a significant increase in IgM level in group I (312.82 ± 46.2) compared with group II (287.1 ± 50.99). However, there was a nonsignificant increase in IgG level in group I (2068.6 ± 306.0) compared with group II (2163.3 ± 360.8). Concerning CD3 level, our study showed that there was a significant increase in CD3 level in group I (62.53 ± 14.35) compared with group II (54.5 ± 15.7).

Finally, we found that there was a highly significant increase in TLC level in group I (25.2 ± 7.04) compared with group II (15.8 ± 3.3).

Al-Saadi et al. [20] found the same result as regards the IgM and IgG levels. However, he found that T-cell counts decreased significantly (P < 0.05) in bacteremic patients than in nonbacteremic patients with diabetes, indicating the effect of bacteremia on the proliferation and function of T cells that leads to immunosuppression of cellular immunity in diabetic patients, thus decreasing T-lymphocyte count.

On the other hand, Martinot et al. [31] found that humoral deficiency is frequent in patients with S. pneumoniae complicated with bacteremia, and Ig dosage should be proposed systematically after such infections, because both IgM and IgG levels were considered as protective antibodies, and their increase indicates colonization; however, in complicated cases with bacteremia in the case of infection with S. pneumonia, both IgM and IgG levels will not act as protective antibodies, and their level might decrease in association with the occurrence of bacteremia.

In our result, the ROC curve showed that with regard to IgM level in diabetic patients, at a cutoff point of 294.95, the sensitivity was 82.5%, specificity was 60%, and accuracy was 75%. Therefore, it had a significant role in the diagnosis of bacteremia in diabetic patients. We also found that at a cutoff point of 1905.45 the sensitivity of IgG for diagnosis of bacteremia in diabetic patients was 75%, specificity was 40%, and its accuracy was 63.3%. For CD3 level, the sensitivity for diagnosis of bacteremia in diabetic patients was 75%, specificity was 55%, and its accuracy was 68.3% at a cutoff point of 56.5.

This was matched by Hasibi et al. [32], who found that the area under ROC curve for distinguishing between cases of bacteremia and healthy controls was larger for IgG compared with IgM. Therefore, IgG level was more reliable than IgM in diagnosis of human bacteremia. The sensitivity was 92.9% and specificity was 100% for IgG level. In addition, Dessau [33] found that combined IgG and IgM levels showed a high and comparable discriminatory ability to distinguish serum samples from patients with bacteremia and controls. However, cutoff values should be adjusted for a proper comparison. In addition, Verkaik et al. [34] reported that IgM and IgG levels help in diagnosis of staphylococcal bacteremia, as 92% of adult bacteremic patients had a marked increase in IgG level, whereas the increase of IgM level was less detected than that of IgG. Finally, Lin et al. [35] reported that we can depend on CD3 and T-lymphocyte subtypes in diagnosis of different types of infections including bacteremia, as an elevated level of CD3 can be used as a predictor infection.


  Conclusion Top


DM, a common disease in a developing country such as Egypt, increases the incidence of bacteremia and worsens its prognosis.

Our results, by the aid of blood culture technique and determination of the antibiotic sensitivity pattern of the isolated organisms, proved that the most common isolated microorganism from blood of diabetic patients with bacteremia was S. aureus.

Our data shed light on the importance of estimation of the level of immunological markers (CD3 by flow cytometry and IgM and IgG by radioimmunodiffusion) in prediction of bacteremia.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

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