A Hospital-Based Study of Epidemiological and Clinical Data on Blastocystis hominis Infection

Abstract

Blastocystis hominis is a foodborne protozoan found in the human feces worldwide. One hundred and ninety-nine individuals with stool samples positive for B. hominis were identified from a pool of 14,325 patient stools collected between 2003 and 2010 from Srinagarind hospital in Thailand. The medical records of patients were reviewed for demographic and clinical data. Of the 85 patients (42.7%) who had B. hominis infection with no co-infections, 42.5% experienced gastrointestinal symptoms. Abdominal pain is the most frequently observed symptom followed by diarrhea. Strongyloides stercolaris and Opisthorchis viverrini were the predominant parasitic co-infections in blastocystosis patients. The infection rates of B. hominis were high during the rainy season. Most B. hominis–infected patients (94%) had underlying diseases; malignancy and chronic diseases were equally top ranked (35.3%) which indicated that B. hominis is an opportunistic protozoan.

Introduction

B lastocystis hominis is a foodborne protozoan found in human feces worldwide. Prevalence of blastocystosis varies among countries; it can be as high as 10% and 50% in developed and developing countries, respectively (Tan et al., 2002; Thathaisong et al., 2003; Boorom et al., 2008; Eroglu et al., 2009). The pathogenicity of B. hominis is inconclusive, due to contradictory reports that it is a commensal protozoa found in fecal samples and the controversial nature of B. hominis as a human pathogen whose infection is correlated with skin rash, abdominal pain, constipation, diarrhea, alternating diarrhea and constipation, irritable bowel syndrome, vomiting, and fatigue (Qadri et al., 1989; Boorom et al., 2008). Some articles have reported that B. hominis does not cause any symptoms (Stenzel and Boreham, 1996; Coyle et al., 2012). This article describes a hospital-based study on the epidemiological data and clinical features of B. hominis–infected patients.

Materials and Methods

Study samples

We retrospectively reviewed the results of all stool examinations at Srinagarind Hospital, between 2003 and 2010. Srinagarind Hospital is a 1,000-bed tertiary-care facility of the Faculty of Medicine, Khon Kaen University, Thailand. Fecal samples of patients from outpatient departments and hospitalized patients requested by clinicians were examined and diagnosed for the presence of intestinal protozoa and helminths by a standard formalin ethyl acetate concentration technique (FECT). The medical records of blastocystosis patients were reviewed.

The results of stool examination of 150 healthy controls were used to compare the rate of B. hominis infection.

FECT technique

The FECT technique (Elkins et al., 1986) was applied to all samples. Briefly, 2 g of individual fecal samples was suspended in a container of 10 mL of normal saline solution (NSS). The suspension was strained through two layers of gauze into a 15-mL centrifuge tube and centrifuged at 700×g for 5 min, and the supernatant was then decanted. Next, 7 mL of 10% formalin was added to the sediment, mixed well, and allowed to stand for 2 min. Then, 3 mL of ethyl acetate was added. The tube was closed, vigorously shaken for 1 min, and centrifuged at 700×g for 5 min. The debris plug in the ethyl acetate layer was loosened, and the top three layers were discarded leaving the sediment. One milliliter of 10% formalin was then added to re-suspend the sediment and examined for parasites under a compound microscope.

Data analysis

The medical records of patients with B. hominis infection were reviewed for demographic and clinical data. Descriptive data of B. hominis–infected patients were accessed to establish the distribution of gender, age group, season, underlying diseases, and co-morbidities. The month of sample reception was used to classify samples as either the wet season (May to October) or the dry season (November to April). The characteristics and laboratory findings of single B. hominis–infected patients with and without gastrointestinal (GI) symptoms were compared by descriptive statistics. The term “gastrointestinal symptoms” in this study refers to any combination of the following symptoms caused by B. hominis infection: abdominal pain, diarrhea, flatulence, anorexia, nausea and vomiting. These symptoms were not related to the patient's underlying disease if presented or not suggestive for acute bacterial or viral gastroenteritis such as acute fever, white or red blood cells in the stool, or a positive rectal swab culture.

Statistical analysis

Data were analyzed and presented by descriptive statistics. Clinical features of those patients with and without GI symptoms were compared by the Student t test, Wilcoxon rank sum test, Chi-square test, or Fisher Exact test where appropriate. The rates of B. hominis infection were compared between patients in the years 2003–2010 and 150 healthy controls. The statistical analysis was done by the STATA package version 10.1. This study was approved by the Khon Kaen University Ethics Committee for Human Research (HE531382).

Results

Overall infection rate

During the study period, there were stool samples from 14,325 patients. Of those, 199 patients had B. hominis infection (1.4%), while there was no B. hominis infection in 150 healthy controls (p=0.276).

Characters of B. hominis–infected patients and infection rate

B. hominis infection was most prevalent in patients with an education level lower than primary school (61.2%), those who worked as farmers (60.4%), and those who lived in a rural area (72.4%). The infection rate of B. hominis between 2003 and 2010 is shown in Table 1. The infection rate declined after the year 2006 despite the increasing numbers of patient stools being tested. In total, the infection rate was 54.3% for males with no differences in gender distribution except in the years 2009 and 2010. The infection rate was high during the wet season (May to October) except in the year 2009, with a mean of 60.3% (Table 1). The infection rates were highest during the rainy season and reached peaks of 11.5% in June and 12.6% in July (data not shown). The mean age±SD of B. hominis–infected patients was 49.2 years±17.8, with a range of 8–90 years. Infection was most common in the age range of 41–50 years, which accounted for 23.6% of all infections (Table 2).

Table 1.

Prevalence of Blastocystis hominis Infection Among Different Demographic Groups During 2003–2010

	Year
Number of	2003	2004	2005	2006	2007	2008	2009	2010	Total
Patients examined stool by FECT (% of total)	642 (4.5%)	962 (6.7%)	1,485 (10.4%)	1,998 (13.9%)	2,086 (14.6%)	2,204 (15.4%)	2,342 (16.3%)	2,606 (18.2%)	14,325 (100%)
Patients positive for B. hominis (%)	20 (3.1%)	29 (3.0%)	44 (3.0%)	48 (2.4%)	10 (0.5%)	24 (1.1%)	12 (0.5%)	12 (0.5%)	199 (1.4%)
Males with B. hominis infection (%)	10 (50.0%)	16 (55.2%)	26 (59.1%)	26 (54.2%)	8 (80.0%)	13 (54.2%)	4 (33.3%)	5 (41.7%)	108 (54.3%)
B. hominis–infected patients in the rainy season^a (%)	14/20 (70.0%)	17/29 (58.6%)	25/44 (56.8%)	29/48 (60.4%)	6/10 (60.0%)	16/24 (66.7%)	4/12 (33.3%)	9/12 (75.0%)	120/199 (60.3%)

Rainy season includes May, June, July, August, September, and October.

FECT, formalin ethyl acetate concentration technique.

Table 2.

Age Distribution of Blastocystis hominis–Infected Patients

Age range (years)	Number (%)
1–10	2 (1.0)
11–20	10 (5.0)
21–30	22 (11.1)
31–40	26 (13.1)
41–50	47 (23.6)
51–60	35 (17.6)
61–70	32 (16.1)
71–80	20 (10.1)
81–90	5 (2.5)

Among the 199 B. hominis–infected patients, 187 (94%) had underlying diseases. The most frequently observed underlying diseases (66/187; 35.3%) were equally prevalent: malignancy and chronic diseases (Table 3). Hematologic malignancy was the most common (32/66; 48.5%) with high frequencies of non-Hodgkin lymphoma (11 patients) and acute myeloplastic leukemia (five patients) (Table 4). Other chronic diseases found in B. hominis–infected patients included diabetes mellitus, hypertension, and heart diseases (25.8%, 21.2%, and 21.2%, respectively) (Table 5). We found that a high number of B. hominis–infected patients were potentially immunocompromised: 61/199 (30.7%) received high doses and/or prolonged use of corticosteroids, 52/199 (26.1%) received chemotherapy, and 12/199 (6%) received radiation therapy. Out of 199 B. hominis–infected patients, 114 (57.3%) were infected with one or more intestinal parasites; Strongyloides stercolaris (57%) and Opisthorchis viverrini (45.6 %) were the first and second most-detected parasites in these patients (Table 6).

Table 3.

Underlying Diseases in the 187 Patients Infected with Blastocystis hominis (Including Single B. hominis and Co-infection with Other Parasitosis)

Underlying diseases	Case (%)
Malignancy	66 (35.3)
Chronic diseases^a	66 (35.3)
Autoimmune and/or connective tissue diseases	35 (18.7)
Eye and skin diseases with steroid treatment	13 (7.0)
Other diseases^b	9 (4.8)
Viral infections^c	5 (2.7)
Hypereosinophilia	5 (2.7)
Irritable bowel syndrome	3 (1.6)

Chronic diseases include diabetes mellitus, hypertension, heart disease, tuberculosis, kidney diseases, lung diseases, thalassemia, and gouty arthritis.

Other diseases include melioidosis, diverticulitis, alcoholism, asthma, spondylosis, malnutrition, and growth hormone deficiency.

Viral infections include hepatitis C virus, hepatitis B virus, herpes zoster virus, and human immunodeficiency virus.

Table 4.

Type of Malignancies Found in 66 Patients Infected with Blastocystis hominis

Type of malignancy	Cases (%)
Hematologic malignancy^a	32 (48.5)
Lung cancer	8 (12.1)
Liver cancer (cholangiocarcinoma and hepatocellular carcinoma)	5 (7.6)
Reproductive system cancer	5 (7.6)
Kidney cancer	4 (6.1)
Gastrointestinal cancer (stomach, colorectal cancer)	4 (6.1)
Brain and metastasis cancer	3 (4.5)
Skin and musculoskeletal malignancy	2 (3.0)
Thyroid cancer	1 (1.5)
Breast cancer	1 (1.5)
AIDS-associated Kaposi sarcoma	1 (1.5)

Hematologic malignancy include non-Hodgkin lymphoma (11), Hodgkin lymphoma (2), lymphoma (3), acute myeloplastic leukemia (5), chronic myeloplastic leukemia (1), acute lymphocytic leukemia (1), chronic lymphocytic leukemia (1), aplastic anemia (2), multiple myeloma (3), histiocytoma (1), and myelodysplastic syndrome (2).

Table 5.

Chronic Diseases Found in 66 Patients Infected with Blastocystis hominis

Chronic diseases	Cases (%)
Diabetes mellitus	17 (25.8)
Hypertension	14 (21.2)
Heart diseases	14 (21.2)
Tuberculosis	8 (12.1)
Chronic kidney diseases	5 (7.6)
Chronic lung diseases	4 (6.1)
Thalassemia	2 (3.0)
Gouty arthritis	2 (3.0)

Table 6.

Parasitic Co-infections Found in 114 Patients Infected with Blastocystis hominis

Co-infected parasites	Cases (%)
Strongyloides stercolaris	65 (57.0)
Opisthorchis viverrini	52 (45.6)
Hookworm	8 (7.0)
Minute intestinal fluke	7 (6.1)
Taenia spp.	3 (2.6)
Echinostoma spp.	3 (2.6)
Trichuris trichiura	2 (1.8)
Entamoeba coli	8 (7.0)
Trichomonas spp.	4 (3.5)
Giardia lamblia	2 (1.8)
Sarcocystis spp.	2 (1.8)
Iodamoeba buetschlii	1 (0.9)

Characteristics of B. hominis–infected patients with and without GI symptoms

Of 199 infected patients, 85 patients (42.7%) had single B. hominis infections and 42.5% (34/80) experienced GI symptoms; five patients are missing these data. Figure 1 lists the GI symptoms in single B. hominis–infected patients. The symptoms observed in these patients (in order of most to least frequent) were abdominal pain (67.6%), diarrhea (50%), anorexia (32.4%), flatulence (29.4%), nausea (14.7%), and vomiting (8.8%). These GI symptoms were not related to the patients' underlying diseases (Table 7). Characteristics of patients who had or did not have GI symptoms are presented in Tables 7 and 8. Patients with GI symptoms were generally male and had more underlying disease entities like hematologic malignancy, HIV infection, or radiation therapy, and loose and mucus-like stools. Those without GI symptoms more frequently had chemotherapy and corticosteroid treatment. There were no characteristics and laboratory findings different between those with or without GI symptoms, except for serum chloride level (p=0.046).

FIG. 1.

Gastrointestinal symptoms found in 34 patients infected with single Blastocystis hominis.

Table 7.

Characteristics of Blastocystis hominis–Infected Patients Comparing Those With and Without Gastrointestinal (GI) Symptoms

Characteristics	With GI symptom N=34 (%)	Without GI symptom N=46 (%)	p-value
Age, years (mean±SD)	46.35±18.9	45.11±18.4	0.768
Male gender	17 (50%)	17 (37%)	0.262
Education level (primary school or lower)^a	15/31 (48.4%)	18/36 (50%)	0.991
Farmers or labor worker^a	16/31 (51.6%)	22/40 (55%)	0.899
Lived in a rural area	25 (73.5%)	38 (82.6%)	0.410
Rainy season	24 (70.6%)	28 (60.9%)	0.478
Had underlying diseases	28 (82.4%)	43 (93.5%)	0.159
Hematologic malignancy	8 (23.5%)	7 (15.2%)	0.394
HIV infection^a	2/9 (22.2%)	0/9 (0%)	0.471
Radiotherapy	4 (11.8%)	3 (6.5%)	0.451
Chemotherapy	9 (26.5%)	15 (32.6%)	0.627
Corticosteroid treatment	9 (26.5%)	17 (37%)	0.346

Data were missing in some patients.

Table 8.

Laboratory Findings Including Complete Blood Cell Count (CBC), Blood Chemistry, and Stool Examination in Blastocystis hominis–Infected Patients Comparing Those With and Without Gastrointestinal (GI) Symptoms

Laboratory finding	GI symptoms Mean±SD	Without GI symptoms Mean±SD	p-value
CBC/no. of sample	29	42
Hemoglobin	11.15±2.5	10.57±2.2	0.300
White blood cell	13.56±14.8	11.79±9.1	0.535
PMN	63.67±18.6	61.5±21.1	0.656
Lymphocyte	22.27±13.6	21.83±13.0	0.889
Monocyte	6.52±4.3	5.78±3.1	0.406
Eosinophil	4.44±7.1	5.49±5.8	0.498
Absolute eosinophil count	566.2±1222.3	528.3±702.1	0.871
Blood chemistry/no. of sample	24	33
Sodium	134.8±4.8	136.0±4.8	0.324
Potassium	4.0±0.6	4.1±0.5	0.771
Chloride	99.2±4.8	102.0±5.3	0.046
HCO₃	24.6±4.4	25.2±3.5	0.554
Albumin	3.2±0.8	3.5±0.6	0.150
Globulin	3.6±0.7	3.8±1.0	0.676
Stool examination/no. of sample	29	37
Loose stool; N (%)	9 (31%)	7 (18.9%)	0.678
Gross mucous stool; N (%)	4 (13.8%)	1 (2.7%)	0.160
Stool occult blood; N (%)	4 (13.8%)	6 (16.2%)	1.000

Discussion

The prevalence of B. hominis in Thailand varies among the provinces as follows: Bangkok, 17.4% (Yaicharoen et al., 2005); Nakhon Pathom, 6.2% (Warunee et al., 2007); and Nakhon Ratchasima, 5.6% (Kitvatanachai et al., 2008). This study showed that the overall frequency of B. hominis infection in a tertiary hospital is 1.4%. The frequency of Blastocystis detection in our laboratory samples by FECT was steady (0.5–1.1%) during the years 2007–2010. Our hospital-based study reported a lower prevalence than the previously mentioned population studies. Previous studies that were examined using different parasitological detection methods (Yaicharoen et al., 2005) or conducted in rural areas and in schools revealed a high prevalence of B. hominis (Warunee et al., 2007; Kitvatanachai et al., 2008). Other hospital-based studies may have shown a higher prevalence of blastocystosis compared to this study because those studies were conducted on patients with GI symptoms (Rostami Nejad et al., 2010; Gonzalez-Moreno et al., 2011; Inceboz et al., 2011; Paschke et al., 2011). FECT, as used for other protozoa and fecal parasites, generally appears to be unsuitable for B. hominis because it causes disruption of the organism (Stenzel and Boreham, 1996). Therefore, cases with small numbers of B. hominis may not be detected.

In this study, the rate of B. hominis infection is slightly higher in men (54.3%). The age distribution was quite normal with the peak in patients aged 30–70 years. The highest infection rates are in the rainy season, and our results are the first report of the seasonal distribution of B. hominis infection in Thai patients. The occurrence of B. hominis infections has previously been related to weather conditions, with the suggestion that infections are more common during hot weather (el Masry et al., 1990; Stenzel and Boreham, 1996) or during the pre-monsoonal months (Babcock et al., 1985). This study shows that the high infection rates in the rainy season reached their peaks in June and July. However, these data do not essentially negate possible dry prevalence peaks. Exposure, experiencing symptoms, seeking medical help, and testing may explain this time lag.

Fecal samples from 150 participants who enrolled in an annual check-up program at Srinagarind Hospital were examined by FECT, and no B. hominis was detected. Most B. hominis–infected patients (94%) had underlying diseases; malignancy and chronic diseases were equally most prevalent (35.3%). In addition, this protozoa was commonly found in patients who received chemotherapy, radiation therapy, and corticosteroid treatment, which may indicate that B. hominis is an opportunistic protozoa.

In some previous reports (Amin, 2002; Kulik et al., 2008), B. hominis was always found to be co-infected with other parasites. Thus, it was not surprising when S. stercolaris and O. viverrini were the two most common co-infection parasites in this study due to the high prevalence of these parasites in the studied area. Co-infection might be related to poor sanitation or the route of transmission (fecal-oral route). Most infected patients had low education (93/152, 61.2%), worked as farmers (110/182, 60.4%), and lived in a rural area (144/199, 72.4%; data not shown).

Humans become infected with B. hominis by the fecal-oral route, and the parasites live in the large intestine. Even though there are still doubts regarding whether B. hominis is a pathogen, GI symptoms due to the infection might occur. In this present study, GI symptoms occurred in 42.5% of patients with B. hominis infection. We found that non-specific abdominal pain was the most common symptom in patients with only B. hominis infection. Previous reports (Qadri et al., 1989; Boorom et al., 2008) indicated that B. hominis was the most common parasite found in patients presenting GI symptoms such as abdominal pain, diarrhea, anorexia, flatulence, and nausea/vomiting, all of which were reported in our study.

Comparison of the characteristics of B. hominis–infected patients with and without GI symptoms showed no statistically significant differences except in serum chloride levels (p=0.046). We have found no hypothesis to explain why the serum chloride parameter was significantly different between those patients with or without GI symptoms. The GI symptoms may depend on the subtypes of B. hominis, which have different pathogenicities (Stensvold et al., 2010; Vassalos et al., 2010; Santin et al., 2011) or depend on human immune status. Due to no clinical differences between patients with or without GI symptoms, we recommend to do a routine stool sample test for B. hominis in patients with any underlying diseases, GI symptoms, or receiving immunosuppressant medication.

The limitation of this study is a retrospective study design. Our laboratory unit used a standard FECT for detection of parasites in the fecal samples because it is accepted as a standard concentration technique for detection of protozoa and helminths in the feces, although in vitro cultivation is more sensitive than FECT in detection of B. hominis. The rate of B. hominis infection may be higher than we reported. The infection rates were based on numbers of stool examination samples. The rates may not apply for general population but represent the hospital-based rates. The causative correlation of GI symptoms and B. hominis infection in this study was not investigated nor reported due to the retrospective design. Further study is needed to define the causative relation of B. hominis infection and specific GI symptoms.

Conclusion

Blastocystis is common in patients with underlying diseases and can cause GI symptoms in 42.5% of patients. The clinical features of B. hominis–infected patients with or without GI symptoms are comparable.

Footnotes

Acknowledgments

This work was supported by the Higher Education Research Promotion and National Research University Project of Thailand, the Office of the Higher Education Commission, and the Faculty of Medicine, Khon Kaen University, Thailand. W.M. and P.M.I. were supported by TRF Senior Research Scholar Grant, Thailand Research Fund (Grant No. 5580004).

Disclosure Statement

No competing financial interests exist.

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