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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2011  |  Volume : 22  |  Issue : 2  |  Page : 237-244
Entamoeba histolytica/Entamoeba dispar infection in chronic hemodialysis patients

1 Faculty of Medicine, Federal University of Uberlandia, Uberlandia, Brazil
2 Faculty of Biological Sciences, Federal University of Uberlandia, Uberlandia, Brazil
3 Clinical Research Unit/Nefroclínica, Uberlandia, Brazil

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Date of Web Publication18-Mar-2011


To determine the prevalence of Entamoeba histolytica/E. dispar (Eh/Ed) in chronic hemodialysis (HD) patients, we collected 330 samples of feces from 110 patients, and nine indivi­duals were found to be positive for Eh/Ed. We compared the infected patients with a group of 14 uninfected HD patients. Both groups were analyzed for their signs, symptoms and socio-economic characteristics using questionnaires. Blood tests were also performed in both the groups. Although both groups did not differ statistically with respect to their signs, symptoms and socio-economic conditions, there was a trend toward a greater number of individuals with diarrhea in the Eh/Ed infected group. In conclusion, we suggest that a parasitological examination of the patient's stool to detect the Eh/Ed complex should be included with the routine tests so that those patients with a positive fecal test could be initiated on appropriate anti-Eh/Ed therapy.

How to cite this article:
Ferreira-Filho SR, da Costa Braga FC, de Sa DM, Nunes EB, Parreira Soares JS, Padovese SM, de Oliveira AC, Ferreira Oliveira GM, dos Passos G, Lemes HP. Entamoeba histolytica/Entamoeba dispar infection in chronic hemodialysis patients. Saudi J Kidney Dis Transpl 2011;22:237-44

How to cite this URL:
Ferreira-Filho SR, da Costa Braga FC, de Sa DM, Nunes EB, Parreira Soares JS, Padovese SM, de Oliveira AC, Ferreira Oliveira GM, dos Passos G, Lemes HP. Entamoeba histolytica/Entamoeba dispar infection in chronic hemodialysis patients. Saudi J Kidney Dis Transpl [serial online] 2011 [cited 2020 Jun 6];22:237-44. Available from: http://www.sjkdt.org/text.asp?2011/22/2/237/77597

   Introduction Top

Patients with chronic renal failure (CRF) on dialysis treatment have a reduced immune res­ponse to various antigens, [1],[2],[3],[4],[5],[6],[7],[8],[9] such as inadequate response to vaccinations. [10],[11] Sepsis-related death is between 100 and 300-times more fre­quent in patients undergoing hemodialysis (HD) compared with the general population [12] of im­portant infections such as Mycobacterium tuberculosis[13] and hepatitis B and C viruses and the immunodeficiency virus (HIV). [14],[15],[16],[17],[18],[19] More­over, infectious diseases occupy the second leading cause of death in this population. [20]

There are little data concerning the contribu­tion of intestinal parasitic infections to protein calorie malnutrition and changes in the im­mune response. [21],[22],[23],[24] Entamoeba histolytica is in­volved in the formation of abscesses in diffe­rent body systems. [25],[26],[27],[28] The clinical manifes­tations of patients with E. histolytica infec­tions, without other associated comorbidities, are highly variable. Most of these infected pa­tients show no symptoms, while a small propor­tion of them manifest with diarrhea, fever and liver abscesses. [29]

Diagnosing E. histolytica infection solely through an optical microscope analysis of the patient's fresh feces is very difficult because of the similarity with the related species, E. dispar. While an invasive character is only as­signed to E. histolytica, there are no data demonstrating that E. dispar could promote health damage in humans. However, experimental studies have shown that an association with other pathogens was able to promote signi­ficant cellular damage. [30],[32],[33],[34] HD patients often have clinical complaints similar to individuals with amebiasis, especially with regard to the gastrointestinal symptoms, such as changes in the number of defecation and the consistency of the feces. [35]

We aim in this study to determine the clini­cal, laboratory and radiological findings in HD patients infected with the Eh/Ed complex in addition to the potential risk factors for ame­biasis and the prevalence of intestinal parasites in HD patients.

   Patients and Methods Top

After approval by the ethics committee of the Federal University of Uberlandia, 110 of the 175 patients with chronic renal failure on HD treatment in the Nefroclinica of Uberlandia, Minas Gerais between March 2005 and April 2007 were recruited into this study. Three stool samples were collected from each patient on different days, and a total of 330 samples were evaluated. All samples were examined by direct microscopy using the method of Hoff­man. [36] Patients whose fecal samples were po­sitive for Eh/Ed complex were subjected to clinical study and laboratory investigations, in­cluding abdominal ultrasound. They were com­pared with HD patients who were negative for both Eh/Ed on stool examination. The search for potential risk factors for an Eh/Ed infection was performed using a questionnaire developed specifically for this study.

The distinction between Eh and Ed by PCR was not one of the endpoints of this study.

   Statistical Analysis Top

The data were entered into the Epidata soft­ware. [37],[38] Data analyses were performed using the EpiInfo [39] and BioEstat softwares. [40] Statisti­cal analyses were conducted in accordance with the following steps. First, the distribution of the frequency of variables was collected for the study population and for the consistency of the data. Next, the distribution of the frequencies of all of the variables was calculated, charac­terizing the study population according to de­mographic and economic factors related to the participant's exposure. Univariate analysis for the household questionnaire was divided into two phases: (1) the demographic variables and the infrastructure of the home were assessed, and (2) the behavioral variables and hygiene were assessed. A univariate analysis was used to test the binomial to compare the two pro­portions (non-parametric test), and an odds ratio (OR) with a 95% confidence interval was used to quantify the association between the risk factors and the investigated Eh/Ed infection. Multivariate analysis was conducted using the logistic regression model in the following se­quence: the variables were selected from the univariate analysis, and all of those considered biologically important with respect to the Eh/ Ed infection (i.e., categorical variables) were transformed into dummy variables.

   Results Top

The study included 110 patients, consisting of 69 males and 41 females. The average age of the group was 52.1 ± 4.6 years, and the duration of hemodialysis treatment was 3.2 ± 1.6 years. Of the study subjects, 96 were re­sidents of Uberlandia and 14 were from neigh­boring towns. The initial results are shown in [Figure 1]. The Eh/Ed complex was the most co­mmon parasite observed during the examination of the subjects' fresh feces, corresponding to 8.2% (nine patients) of all the patients exa­mined. In both the study group and the con­trols, no patient presented with fever or hepa­tomegaly at the time of the study. Among the five patients in the Eh/Ed-positive group that were also surveyed for ultrasonography, none had a liver abscess, and among the 13 control subjects, none were found to have any signi­ficant liver changes. Only one patient in the Eh/Ed-positive group had eosinophilia, while five patients in the control group had eosino­philia. Anemia was identified in 85.7% of pa­tients in the Eh/ Ed-positive group and in 100% of the controls [Table 1]. In the univariate ana­lysis of the studied clinical variables, no varia­ble presented a significant difference between the Eh/Ed-positive group and the controls [Table 1]. The univariate analysis for the household questionnaire was divided into two phases. In the first phase, the demographic variables and infrastructure of the household were assessed [Table 2], and in the second phase, the beha­vioral and health variables were assessed [Table 3]. The investigated variables showed no sta­tistically significant differences between the Eh/Ed-positive group and the controls. The household survey showed that none of the investigated variables had a P <0.25 and, thus, it was not possible to construct a logistic re­gression model with potential clinical risk fac­tors for infection by Eh/Ed among the HD pa­tients. As none of the investigated variables were significantly changed (P < 0.05, 95% CI), it was not possible to construct a final multi­variate logistic model.
Figure 1: Distribution of intestinal parasites found in hemodialysis patients (n=110).

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Table 1: Distribution of the cases and controls for Entamoeba histolytica/Entamoeba dispar with respect to the secondary clinical variables between patients undergoing hemodialysis.

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Table 2: Distribution of the cases and the controls for Entamoeba histolytica/E. dispar for the secondary demographic variables and home infrastructures in hemodialysis patients.

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Table 3: Entamoeba histolytica/E. dispar: Hygienic conditions among patients undergoing hemodialysis (positive cases versus controls).

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Of the nine patients who formed the group of Eh/Ed-positive cases, one underwent a kidney transplant and two died of cardiovascular cau­ses during the study period; however, one of these patients had already responded to the questionnaires. Thus, the medical histories and interviews were conducted in seven of the pa­tients from the Eh/Ed-positive group. In the control group, one patient also died from car­diovascular causes and another changed to another form of dialysis; thus, leaving the study protocol. We inserted two new non-infected patients with similar characteristics to those who left the study, and then we conducted in­terviews with the 14 control patients, as re­quired. None of the three deaths from the Eh/ Ed-positive patient group were related to com­plications of the Eh/Ed infection.

   Discussion Top

Our data show that 8.2% of the population on hemodialysis was infected with the Eh/Ed complex. We did not observe any differential signs or clinical symptoms in the patients with and without the intestinal parasite. The social conditions in which the Eh/Ed-positive pa­tients lived were also not different from those presented by the control group. Accordingly, it is unlikely that the hygienic conditions of the positive patients were a factor in their infec­tion, as both studied groups of patients had good structures of water and sewage in their residence. During the study period, there were no significant differences in weight loss, epi­sodes of fever, vomiting and abdominal pain.

Despite the fact that the microscopic exami­nation of the fresh feces of patients - to search for cysts and/or trophozoites is considered the most common method for diagnosing intes­tinal amebiasis - this procedure is being re­assessed for its efficacy since the discovery of another non-pathogenic species of Entamoeba. A reclassification was made by Huston and Petri in 1999, when they defined Entamoeba histolytica as a pathogen and Entamoeba dis­par was defined as non-pathogenic and unable to cause disease to its host. [41] This reclassi­fication was based on the different aspects of clinical, biochemical, immunological and ge­netic characteristics found between these two protozoans. Since E. dispar is ten-times more prevalent than E. histolytica, the inability to differentiate between both protozoa may lead to unnecessary treatments. However, there is some experimental evidence that demonstrates that E. dispar can become pathogenic in cer­tain special situations. [42],[43],[44],[45] In addition, the la­boratory tests needed to correctly identify both protozoa are expensive to be applied routinely.

Another topic, often pursued by physicians diagnosing an intestinal parasite infection, is the presence of eosinophilia in the infected patients. [46] Eosinophilia was present in both groups, and the number of cases in each group was not significantly different (P > 0.05). The presence of eosinophilia could be attributed to the fact that all the HD patients had contact with several artificial substances, such as ca­theters and intravenous blood lines. It is also possible that manufactured products used in the dialysis process can promote an increase in the number of eosinophils in blood.

With respect to the patients' family income, the data show that the incomes in both the HD patient groups were not significantly different. The subjects in both groups also consumed filtered water, had a sewage network in their residence and consumed vegetables only after cleaning. Although the city of Uberlandia in Brazil is situated in a developing country, it has adequate service for the treatment of water and sewage, which may explain the absence of statistical differences in these variables.

Despite the fact that there was no statistical significance in the values, diarrhea occurred in 42.9% of the infected group versus 21.4% (NS) of the subjects in the control group. Certainly, the small number of individuals who represen­ted our sample of cases influenced the out­come of the performed statistical analyses. However, there was a tendency for more cases of diarrhea in the Eh/Ed-positive group com­pared with the controls. If this observation is confirmed in future studies that contain a lar­ger sample population, it will be possible to question whether E. dispar may or may not be pathogenic to people undergoing hemodialy­sis. The low-immune competence of these in­dividuals and the possibility of concurrent infections could contribute to this reasoning. HD patients who are positive for the Eh/Ed com­plex could be treated with the appropriate me­dication soon after a positive microscopic diag­nosis, as the risks and benefits analysis would favor the initiation of therapy.

The incidence of the Eh/Ed complex, which is transmitted through the ingestion of conta­minated food and water, is greater in areas with poor hygienic conditions and a low socio­-economic level. [28],[47] However, our data show that physicians should not solely rely upon socio-economic parameters for the diagnosis of intestinal amebiasis, especially in places with an adequate health structure, such as the city where this study was conducted. Factors other than those investigated in this study may be involved in the epidemiology of HD patients.

Limitations of the Study

The introduction of bias is a factor that should be considered, particularly the type of selec­tion process. For example, a sample population with a small number of patients who have si­milar characteristics could have influenced the determination of risk factors that were pre­viously cited in the literature in association with infection with E. histolytica/E. dispar. How­ever, the careful selection of our control group provided comparable features with the positive cases, as they were matched by sex, age and length of dialysis. Therefore, it is believed that this type of bias was not introduced into this study. However, the defect of memory, usually observed in retrospective studies, may have been introduced, and should be considered in the investigated clinical symptoms. For the study part related to the patients' residence, the surveyed factors were not as dependent on memories, which minimized this type of bias.

In conclusion, we suggest that a parasito­logical examination of the patient's stool to detect the Eh/Ed complex should be included with the routine tests so that those patients with a positive fecal test could be initiated on appropriate anti-Eh/Ed therapy.

   References Top

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43.Diamond LS, Clark CG. A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. J Eukaryot Microbiol 1993;40:340-4.  Back to cited text no. 43
44.Vohra H, Bhatti HS, Ganguly NK, Mahajan RC. Virulence of pathogenic and non-patho­genic zymodemes of Entamoeba histolytica (Indian strains) in guinea-pigs. Trans R Soc Trop Med Hyg 1989;83:648-50.  Back to cited text no. 44
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Correspondence Address:
Sebastiáo Rodrigues Ferreira-Filho
Rua Paraíba 3055, Uberlandia
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