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Acta Medica Alanya
2022;6(1): 64-71
DOI:10.30565/medalanya.987899
To cited: Özsan Yılmaz M. Detection of intestinal parasites by different methods in our type 2 diabetic patients. Acta
Med. Alanya 2022;6(1): 64-71 doi:10.30565/medalanya.987899
*Corresponding Author: Müge ÖZSAN YILMAZ, Hatay Mustafa Kemal University Faculty of Medicine,
Endocrinology and Metabolism Department, Hatay, Turkey, +903262291000, mozsan@mku.edu.tr
ORCİD: 0000-0001-8346-8941
Received: 27.08.2021 Accepted: 18.12.2021 Published (Online):27.03.2022
ÖZ
Amaç: Uzun süreli kalıcı yüksek kan şekeri seviyeleri diyabetik hastalarda çeşitli
olumsuz sonuçlara yol açar. Bunlardan bir tanesi gastrointestinal bozukluklar ve
bir diğeri de parazitozlar gibi enfeksiyöz hastalıklardaki risk artışıdır. Bu çalışmanın
amacı diyabetik hastalarda bağırsak parazitlerinin çeşitli tekniklerle gösterilmesi ve
sıklığının belirlenmesidir.
Yöntemler: Çalışmaya 65 tip 2 diyabet hastası dahil edildi. Rutin laboratuvar testleri
yapıldı ve semptomları kaydedildi. Fekal örneklerde direkt mikroskopi, Kinyoun asit
fast boyama, trikrom boyama, hızlı antijen tarama(HAT) teknikleriyle intestinal parazit
arandı.
Bulgular: Çalışmaya dahil edilen hastaların 31’ i erkek, 34’ü kadın cinsiyette idi.
Hastaların %53.8'inde diyabetin kronik komplikasyonu mevcut olmayıp, %33.8'inde
çoklu komplikasyon mevcuttu. Otuz (%46,2) hastada gastrointestinal şikayetler tespit
edildi. Dışkı örneklerinin incelenmesinde HAT ile iki hastada (%3.07) G. intestinalis,
üç hastada (%4.6) C. parvum ve altı hastada (%9.2) G. intestinalis + E. histolytica
tespit edildi. HAT ile belirlenen parazit varlığı ile yaş, cinsiyet, diyabet süresi ve
dispeptik şikayetler gibi hasta özelliklerinden herhangi biri arasında ilişki bulunmadı
(p değerleri sırasıyla 0,27; 0,14; 0,90; 0,68'dir).
Sonuç: Bu çalışma diyabetik hastalarda HAT ile parazitoz prevalansını araştıran
ilk çalışmadır. Ayrıca bu çalışmada bu hasta popülasyonunda farklı parazit tespit
yöntemlerini de karşılaştırdık ve HAT’ın daha sensitif bir yöntem olduğunu gösterdik.
Anahtar kelimeler: Tip 2 Diabetes Mellitus, parazitik bağırsak hastalıkları,
gastrointestinal hastalıklar, antijen, mikroskopİ
ABSTRACT
Aim: Long term persistently high blood glucose levels result in various complications
and conditions in diabetic patients. One of them is gastrointestinal disorders and the
other is increased risk of infectious diseases like parasitosis. The aim of the study is
to demonstrate of intestinal parasites with various techniques in diabetic patients and
conrm of the frequency of the parasites.
Methods: A total of 65 patients with type 2 Diabetes Mellitus were included in the
study. Laboratory tests were done and gastrointestinal symptoms were recorded.
Fecal specimens were evaluated with direct microscopy, Kinyoun acid-fast staining
method, trichrome staining method and antigen screening test.
Results: Of the patients included in the study 31 were male and 34 were female. While
53.8% of the patients had no chronic complications of diabetes, 33.8% had multiple
complications. Thirty (46.2%) patients had gastrointestinal complaints. Examination
of stool samples revealed G. intestinalis in two patients (3.07%) , C. parvum in three
patients (4.6%), and G. intestinalis + E. histolytica in six patients (9.2%) by RAT. No
association was found between the existence of parasite determined by RAT and
any of the patient characteristics of age, sex, duration of diabetes, and dyspeptic
complaints (p-values are 0.27; 0.14; 0.90; 0.68, respectively).
Conclusion: This is the rst study to explore the prevalence rate of parasitosis
detected by RAT in patients with diabetes. In this study, we also compared different
parasite detection methods in this patient population and showed that RAT is a more
sensitive method.
Keywords: Type 2 Diabetes Mellitus, Parasitic Intestinal Diseases, Gastrointestinal
Disorders, antigen, microscopy
1.Hatay Mustafa Kemal University Faculty of Medicine, Endocrinology and Metabolism Department, Hatay, Turkey
Müge Özsan Yılmaz1*
Tip 2 diyabetik hastalarımızda farklı metotlarla intestinal parazitlerin tespiti
Detection of intestinal parasites by different
methods in our type 2 diabetic patients
ARAŞTIRMA
RESEARCH ARTICLE
Acta Medica Alanya 2022:6:1 65
Introduction
Diabetes mellitus is a chronic disorder of
carbohydrate, lipid and protein metabolism
which may result from a total or partial deficiency
of insulin or resistance against insulin action
in peripheral tissues. Long term persistently
high blood glucose levels result in various
complications. Furthermore, in diabetic patients,
the frequency of gastrointestinal (GI) symptoms
is increased. Although the exact pathogenesis of
diabetes related GI disease is not known clearly,
it is thought that the underlying gastroparesis,
depression, and anxiety disorders may induce
these symptoms [1]. It was concluded that poor
glycemic control might increase the frequency of
these symptoms in various studies, albeit with
conflicting results [2].
Diabetes mellitus increases the risk of infections.
Neutrophil chemotaxis, adherence of neutrophil
to the vascular endothelium, phagocytosis,
intracellular bactericidal activity, opsonization,
and cellular immunity are suppressed in case
of persistent hyperglycemia [3]. Because of
these disturbances diabetes may acceptable
as immunodeficiency condition. Immundeficient
patients are more susceptible to infections with
opportunistic parasites such as Entamoeba
histolytica, Cryptosporidium parvum, and Giardia
intestinalis. Host-parasite interactions and a
decline in or loss of host’s resistance to parasites
play a role in the transformation of parasites to the
pathogen status or increase in their pathogenicity
[4].
Amebiasis remains a significant health problem
for developing countries [5]. Humans are
infected by two species of Entamoeba, which
are morphologically indistinguishable. These are
infective E.histolytica and nonpathogen E. dispar.
The differential diagnosis for E.histolytica and E.
dispar can be achieved by the detection of specific
antigens.
Cryptosporidium species are one of the commonly
detected parasites in humans, domestic animals,
and wild vertebrates [6]. While cryptosporidiosis
causes mild diarrhea in immunocompetent
individuals, it can cause life-threatening severe
diarrhea and respiratory system infection in
immunocompromised patients [7].
G. intestinalis is one of the leading culprits of
endemic and epidemic diarrheas globally. The
prevalence of giardiasis varies between 1.9%
– 37.7% in studies conducted in Turkey [8,9].
Giardiasis, which might be seen in acute and
chronic forms, could be asymptomatic and also
cause life-threatening diarrhea.
Several studies were published as to the
diagnosis of intestinal parasites in various patient
groups in our country [4,10-12]. To the best of
our knowledge, there is no study in the literature
studying prevalence rates of amebiasis, giardiasis,
and cryptosporidiosis by Rapid Antigen Test
(RAT) in diabetic subjects. Hence, we aimed to
investigate frequencies of amebiasis, giardiasis,
and cryptosporidiosis in diabetic patients by
means of an antigen screening test and to study
whether there is an association between these
parasites and diabetic gastrointestinal complaints.
We also planned to compare the rate of parasite
presence by different laboratory techniques.
Methods
A total of 65 patients with Type 2 Diabetes Mellitus
and aged 18 to 65 who were assessed at adult
Endocrinology and Metabolism outpatient clinic
between January and June 2016 were included in
this prospective study. An informed consent form
was signed by all patients who were eligible for
the study and wished to participate. The patients
who have any gastrointestinal malignancy and
immunosuppressive condition history or presence
of clinically significant chronic disease other than
diabetes mellitus were excluded. Age, gender,
and concomitant diseases of the patients were
recorded.
Serum glucose, creatinine, aspartate
aminotransferase (AST), alanine aminotransferase
(ALT), sodium (Na), potassium (K), hemoglobin
A1c (HbA1c) and complete blood count (CBC) were
measured in all participants. CBC tests were done
with Mindray BC 6000 (Mindray Co., Shenzhen,
China) a haematology device. Biochemistry
parameters (Glucose, creatinin, AST, ALT, Na, K,
Albumin, Calcium, Phosphorus, Magnesium, Total
cholesterol, HDL cholesterol, LDL cholesterol,
Triglyceride) were studied by spectrophotometric
method in Siemens Advia 1800 biochemistry
autoanalyzer (Siemens, Germany) and HbA1c
Yılmaz MÖ. Diabetes and intestinal parasites
Acta Medica Alanya 2022:6:1 66
Yılmaz MÖ. Diabetes and intestinal parasites
levels were studied by HPLC (High Performance
Liquid Chromatography).
Patients were questioned in detail in terms of
chronic complications of diabetes and the findings
were supported by hospital records. Patients
for whom appropriate and sufficient information
could not be obtained from their anamnesis and
records were screened for chronic complications.
For this purpose, fundus examination was done
for diabetic retinopathy, sensory examination
evaluation of orthostatic hypotension for diabetic
neuropathy, microalbumin level in 24-hour urine
and GFR calculation for diabetic nephropathy,
detailed cardiac examination, Doppler USG for
carotid and peripheral arteries, and angiographic
examinations were performed when necessary.
Patients were questioned regarding
gastrointestinal symptoms such as postprandial
fullness, early satiety, epigastric pain, epigastric
burning, diarrhea, constipation for the last three
months. If the patient had at least one of these
symptoms, it was deemed that the patients had
dyspepsia. Fecal specimens collected from
65 patients were brought to the Parasitology
Laboratory in which direct microscopy results
were obtained by precipitation with native, Lugol’s
iodine and formalin ethyl acetate techniques by
a consultant parasitologist. Samples were also
examined for intestinal parasites using Kinyoun
acid-fast staining method, trichrome staining
method, and antigen screening test.
1-Kinyoun Acid-Fast Staining Method: Smears
were prepared from the collected stool samples
and allowed to dry. Then, they were fixed in pure
methanol for one minute. The smears were stained
with Kinyoun carbol fuchsin for five minutes and
then shaken with 50% alcohol. After that, the
specimens were washed with tap water and held
in a chalet containing 1% sulfuric acid for two
minutes and then washed in the tap water again.
After leaving for one minute in the methylene
blue-containing chalet, they were washed with
the tap water, then dried and examined via 100X
objective of a microscope [13].
2-Conventional Trichrome Staining Method:
Stool samples were spread on the slides. After
the edges of slides began to dry, they were held
in the Schaudinn fixative at least half an hour.
Respectively, they were left in 70% ethyl alcohol
for five minutes, in iodine solution of D’Antoni for
three minutes, in two chalets containing 70% ethyl
alcohol for two and five minutes, and in trichrome
staining solution for eight minutes. Then, excess
dye on the slides was removed. They were soaked
three times in 90% acid-alcohol and shaken in two
chalets containing 95% ethyl alcohol. The slides
were held in two chalets containing carbol-xylene
for two and five minutes, in two chalets containing
xylene for two and five minutes, and then they
were allowed to dry.
3-RIDA Quick Cryptosporidium / Giardia /
Entamoeba Combicasette antigen test (R-Biopharm
AG, Germany) was used as an antigen screening
test. The rapid antigen test (RAT) is a one-step
immunochromatographic lateral flow test. The
specific antibodies themselves directed against
each parasite bind to green (Entamoeba specific),
red (Giardia specific), or blue (Cryptosporidia
specific) latex particles. Other antibodies specific
to these three pathogens bind firmly to the
membrane. The stool sample is suspended in
the extraction buffer and then precipitates. Clear
supernatant part of the sample is placed on the
test area.
Ethics committee approval of the study was
obtained from Hatay Mustafa Kemal University
Tayfur Ata Sökmen Faculty of Medicine Clinical
Research Ethics Committee with the decision
number 131, dated 17.11.2015.
Statistical analysis
Data were recorded to SPSS 21 System with
double check and analyzed using SPSS 21 with
95% confidence. After evaluating normality with
Shapiro Wilk test, Student-t test was used for
normally distributed data and Mann Whitney U
test was used for data not normally distributed. In
categorical data, chi-square tests were used. The
significance limit for all tests was set at 0.05. ROC
analysis was performed to evaluate whether there
would be parasitosis according to the WBC value.
The performance of the assay was calculated
by the area under the curve (AUC) sensitivity
and specificity values. In addition, PPV (positive
predictive value), NPV(negative predictive value),
Sen (Sensitivity) and Spe (Specifity) values were
calculated for RAT when direct microscopy was
Acta Medica Alanya 2022:6:1 67
Yılmaz MÖ. Diabetes and intestinal parasites
accepted as gold standard.
Results
Sixty-five patients with type 2 Diabetes Mellitus
were included in the study. Of all participants,
47.7% (n=31) were males, and 52.3% (n=34)
were females. The mean age of the patients was
51.5 ± 12.3 years. 53.8% of the patients had
hypertension and 52.3% had hyperlipidemia. The
median duration of diabetes mellitus diagnosis
was 7 (1-20) years. While 53.8% of the patients
had no chronic complications of diabetes, 33.8%
had multiple complications. Thirty (46.2%)
patients had gastrointestinal complaints, of which
nineteen (n=19) had dyspepsia and the rest
had constipation or diarrhea. The frequency of
gastrointestinal complaints was 44.1% (n=15) in
women and 45.1% (n=14) in men (p=0.87).
Examination of stool samples revealed C.
parvum in one patient (1.5%) by Kinyoun method,
G. intestinalis + E. histolytica in six patients
(9.2%) by trichrom method, G. intestinalis in
seven patients (10.7%) by direct microscopy, G.
intestinalis in two patients (3.07%) , C. parvum
in three patients (4.6%), and G. intestinalis +
E. histolytica in six patients (9.2%) by RAT. No
association was found between the existence of
parasite determined by RAT and any of the patient
characteristics of age, sex, duration of diabetes,
and dyspeptic complaints (p-values are 0.27,
0.14, 0.90, 0.68, respectively). No association
was found between HbA1c and other biochemical
parameters and the existence of parasite (Table
1). There was not an association between the
presence of parasite and hemoglobin, eosinophil,
and lymphocyte counts (p>0.05). The association
between the number of white blood cells (WBC)
and the existence of parasites was not statistically
significant. However, the frequency of parasite
positivity increased as the number of WBCs
decreased (Table 1). The area under the curve
(AUC) was calculated as 0.711 and p=0.023 in the
ROC analysis based on the presence or absence
of parasites for the WBCs. The cut-off value for
the WBCs was calculated as 6860 /μL with 66%
sensitivity and 77% specificity (Figure 1).
No significant association between the parasite
positivity and diabetic complications such as
diabetic neuropathy, retinopathy, coronary
artery disease, cerebrovascular disease and
comorbidities was found, either (p>0.05) (Table
2).
When the RAT was compared with other methods
in terms of parasite evaluation, the samples
deemed as negative by direct microscopy was
negative in 91.4% of the samples studied with RAT
method, as well. All samples that were considered
as positive by direct microscopy were also found
to be positive with RAT (Table 3).
Figure 1. Association between existence of parasites and white blood cell
count
Discussion
As the number of people with diabetes increases
rapidly the associated complications of diabetes
will increase inevitably. In the long term, diabetes
leads to chronic complications including various
gastrointestinal symptoms in which neuropathy
is an important causative factor. The prevalence
of these symptoms varies according to ethnic
groups and the type of diabetes [1]. While it has
been reported that gastric emptying is delayed in
25-55% of type 1 diabetic patients, and in 30%
of type 2 diabetic patients, the prevalence of
gastroparesis in the community has been reported
to be approximately 5% in Type 1 diabetes and
1% in Type 2 diabetes [14]. In our study, 46.2% of
diabetic patients had gastrointestinal symptoms,
most common of which were dyspepsia and
constipation/diarrhea. Gastrointestinal complaints
related to diabetes are known to be more prevalent
among women. The reason for this difference could
Acta Medica Alanya 2022:6:1 68
Yılmaz MÖ. Diabetes and intestinal parasites
Table1. Association between existence of parasites and biochemical and hemogram results
Parasite (+)* Parasite (-)* p
Mean±SD Median Min-Max Mean±SD Median Min-Max
A1C (%) 8.97±2.24 8.80 6.4-16.4 8.85±1.34 8.80 6.8-11.5 0.899
Glucose (mg/dL) 198.81±79.84 193.00 87-391 176.83±84.49 145.00 100-400 0.290
Creatinin (mg/dL) 0.82±0.14 0.79 0.56-1.39 0.97±0.26 0.90 0.56-1.39 0.029
LDL-chol (mg/dL) 118.58±63.33 104.00 7-363 91.92±42.38 89.50 7-163 0.099
HDL-chol (mg/dL) 41.88±16.61 41.00 13-129 37.83±8.93 40.50 19-51 0.388
Total chol (mg/dL) 209.24±110.08 188.00 78-838 243.42±190.63 192.00 144-838 0.806
Triglyceride (mg/dL) 192.11±144.05 157.00 49-846 218.08±179.2 163.00 68-711 0.919
AST (U/L) 22.21±12.48 18.00 9-67 21.67±5.66 22.00 11-31 0.330
ALT(U/L) 23.79±13.1 17.00 7-60 24.58±7.9 26.00 13-38 0.466
Na (mmol/L) 137.53±2.4 138.00 132-141 136.33±1.72 137.00 134-139 0.058
K (mmol/L) 4.54±0.44 4.40 3.6-5.5 4.45±0.38 4.45 3.6-4.9 0.568
Albumin (g/dL) 3.64±0.25 3.60 3.2-4.3 3.7±0.29 3.75 3.2-4.3 0.388
Ca (mg/dL) 8.97±0.37 9.10 8.4-10.4 9.11±0.51 9.10 8.5-10.4 0.490
P (mg/dL) 3.74±0.62 3.70 2.4-5.2 3.85±0.71 3.66 3-5.2 0.965
Mg (mg/dL) 1.84±0.26 1.80 1.4-2.72 1.84±0.13 1.80 1.56-2.05 0.413
WBC /μL 7191.33±2041.92 6595.00 5200-12070 8669.02±2134.01 8150.00 4400-12970 0.023
Eosinophil /μL 186.67±130.55 160.00 0-450 236.79±170.05 190.00 0-660 0.462
Lymphocyte/μL 2324.17±883.4 2405.00 950-3590 2790.94±1094.55 2830.00 70-6490 0.148
Platelet /μL 255.83±52.82 249.50 176-344 292.62±96.6 265.00 150-554 0.374
*with Rapid Antigen Test, SD: Standard deviation, Min: Minimum, Max: Maximum, LDL-chol: Low density lipoprotein cholesterol, HDL-chol: High
density lipoprotein cholesterol, Total chol:Total cholesterol, AST: Alanine aminotranspherase, AST: Aspartate aminotranspherase, Na:Sodium, K:potassium,
P:Phosfor, Mg:Magnesium, WBC: White Blood Cell, p:Statistical significance for Student-t and Mann-Whitney U tests, p≤0,05
Table 2. Association between existence of parasites and comorbidity,
complications
Comorbidity / Complications n/
percent
Parasite
(-)*
Parasite
(+)*
p
Hypertension (-) n 24 6 0.767
% 80.0 20.0
(+) n 29 6
% 82.9 17.1
Dislipidemia (-) n 24 7 0.414
% 77.4 22.6
(+) n 29 5
% 85.3 14.7
Complications (-) n 29 6 0.263
% 82.9 17.1
Neuropathy n 3 0
% 100.0 0.0
Retinopathy n 0 1
% 0.0 100.0
Coronary arter
disease
n 2 0
% 100.0 0.0
Cerebrovascular
disease
n 1 1
% 50.0 50.0
Multiple
complications
n 18 4
81.8 18.2
Table 3. Association between rapid antigen test and the other tests
Comorbidity / Complications n/
percent
Parasite
(-)*
Parasite
(+)*
p
Kinyoun Negative n 53 11 0.185
% 82.8% 17.2%
C. parvum n 0 1
% 0,0% 100,0%
Trichrom Negative n 53 6 0.001
% 89.8% 10.2%
G. Intestinalis
+ E. histolytica
n 0 6
% 0.0% 100.0%
Direct
microscopy
Negative n 53 5 0,001
% 91.4% 8.6%
G. Intestinalis n 0 7
0.0% 100.0%
*with Rapid Antigen Test, PPV=0.58, NPV=1.00, Sen=1.00 and Spe=0.91
for RAT, PPV: Positive predictive value, NPV: Negative predictive value,
Sen: Sensitivity, Spe: Spesifity, RAT:Rapid Antigen Test, C. parvum:
Cryptosporodium parvum, G. Intestinalis: Giardia intestinalis, E.
histolytica: Entamoeba histolytica n: Number of patients, p:Statistical
significance for Chi-square test, p≤0,05
Acta Medica Alanya 2022:6:1 69
Yılmaz MÖ. Diabetes and intestinal parasites
not be explained clearly yet, but it is associated
with a high prevalence of abdominal bloating/
fullness in women [15]. However, our results
revealed that the prevalence of these complaints
was similar between females and males (44.1%;
45.1%, respectively).
Although the entire pathogenetic process of
gastrointestinal complications of diabetes mellitus
is not well understood; gastroparesis, depression,
and anxiety disorders may impact these
symptoms. The effect of poorly controlled diabetes
on these symptoms is not clear. However, it is
known that the level of glycemic control affects
gastric emptying [1]. Persistent poor glycemic
control may lead to damage to the vagus nerve,
and autonomic neuropathy in diabetic patients.
This process usually takes about ten years [16].
Poor glycemic control can shorten this duration.
However, it is controversial whether it increases
symptoms [1,2]. Although the median duration
of diabetes was seven years in our patients,
higher HbA1c mean value could explain the more
frequent gastrointestinal symptoms in our study
population.
The pathogenesis of functional gastrointestinal
disorders is poorly understood in healthy population
as well as in diabetic patients, however, factors
such as prolonged gastric emptying, tenderness in
stomach tension, and infiltration of the duodenum
with inflammatory cells might impact pathogenesis
[17,18].
Chronic dyspeptic complaints can be observed
following bowel infections. Many pathogens
including G. intestinalis were held responsible
for the development of these complaints [19].
While E. histolytica causes acute abdominal pain
and diarrhea, it may also give rise to abscess
formation throughout the body, especially in the
liver. C. parvum may present as a diarrheal illness
in immunocompromised individuals [4,5]. In our
study, we did not show any association between
the presence of any of the parasites studied and
the symptoms such as dyspepsia, constipation,
and diarrhea. This may be in part due to the small
number of participants in this study.
Parasitic diseases still pose a significant health
problem for underdeveloped and developing
countries. These diseases are among the important
causes of the morbidity and the mortality in these
regions. For example; every year, 50 million
people in the world are infected with amebiasis,
only 10% of them are symptomatic and 100 000
people die [5]. In Turkey, intestinal parasitosis is
common in regions where infrastructure problems
could not be solved, and compliance with personal
hygiene is poor.
Diabetes increases the risk of various infections.
Hyperglycemia and hyperglycemia-induced
reduction in immune response, vascular
insufficiency, peripheral and autonomic
neuropathy, colonization of skin and mucosa with
some microorganisms are among the causes of this
predisposition. Hyperglycemia affects chemotaxis
of neutrophils, adherence to vascular endothelium,
phagocytosis, intracellular bactericidal activity,
opsonization, and cellular immunity favorably [3].
Immunosuppressed patients are more likely to be
infected with opportunistic parasites such as E.
histolytica, C. parvum, and G. intestinalis. Host-
parasite associations and decrease or complete
loss of host resistance to parasites play a role in
the transformation of parasites into a pathogen
or increased pathogenicity [4]. Our results
demonstrated that as the number of WBCs, which
is an indicator of the host’s reaction to parasites,
was lower than approximately 7000/μL, the
prevalence of parasitosis increased.
There are various studies in the literature reporting
the prevalence of different parasites in diabetic
patients. In a study of 100 diabetic patients
from Egypt, G. intestinalis was detected in 22%,
E. histolytica in 7% and C. parvum in 5% of the
patients [20]. In another study involving more
patients, the prevalence of C. parvum was reported
as 8.4% [21]. In another study, the prevalence
of G. intestinalis was 13%, while E. histolytica
was seen in 1% [22]. In a study conducted in
our country, the prevalence of G. intestinalis in
diabetic patients was found to be 15% [23]. In our
study, the prevalence of all parasites combined
was 16.9% studied by RAT, which had the highest
sensitivity among the techniques we utilized. The
prevalence rates of parasites in our study were
4.6% for C. parvum and 3% for G. intestinalis.
The prevalence of G. intestinalis was less than
other studies reported in the literature, for which
a relatively small sample size of our study could
Acta Medica Alanya 2022:6:1 70
Yılmaz MÖ. Diabetes and intestinal parasites
account. In our research, while E. histolytica
was not seen alone, the prevalence of it with G.
intestinalis was 9.2%. The prevalence of multiple
parasitic infestations was higher in our study, as
in other studies [21,22].
Uyar and Taylan Ozkan reported that the diagnosis
of G. intestinalis and other protozoa was usually
made by direct microscopic examination and it
was a cheap technique [24]. However, they stated
that the microscopic examination, especially
by augmentation methods, was demanding and
required experienced staff, and intensive work. On
the contrary, antigen detection methods (Direct
fluorescent antibody-DFA, enzyme immunoassay-
EIA, rapid antigen tests-RAT) are useful in the
diagnosis of protozoa because they are rapid and
do not require experienced staff [24].
Aziz et al. emphasized that immunological methods
such as DFA were more sensitive, useful, faster,
and cost-effective than traditional microscopic
techniques in the diagnosis of G. intestinalis
[25]. Also evident in our patient group, RATs can
provide a practical, early, and safe diagnosis for
immunocompromised patients in centers that do
not have adequate laboratory equipment and
experienced staff.
Limitations of the Study:
Despite the interesting findings, the main and the
first limitation of our study was the sample size. The
sample size available was small. If we had a larger
number of patients, we could have divided them
into subgroups according to the characteristics
of the patients especially for diabetic neuropathy
existence. We could obtain more significant
results in these subgroups in terms of parasitosis.
Second we did not have a control group to account
for the prevalence of parasitosis in the general
population in our region. In addition, we did not
use any objective measure to diagnose specific
types of diabetic gastrointestinal complications
such as gastric emptying study.
Conclusion
Since cellular immunity is defective in diabetic
patients it has been assumed that frequency
of parasitic infestations might increase among
diabetic patients, which is confirmed in some
but not all studies. Our results revealed a similar
frequency of intestinal parasitic infections reported
in the literature; however, it seems that the most
sensitive method to detect these infections is
antigen screening test. With such easy to use
tests, diabetic patients can easily be screened
with this regard. Hence, we can distinguish
gastrointestinal symptoms related to diabetic
intestinal autonomous neuropathy from those
related to intestinal parasites. Parasitosis such as
E. histolytica, C. parvum, G. intestinalis may have
an effect on gastrointestinal problems in diabetic
patients, but large sample studies are required to
demonstrate these associations.
Although we have some limitations in this study on
the other hand it has some strength as well. This
is the first study to explore the prevalence rate of
parasitosis detected by RAT in diabetic patients.
Furthermore, we also compared different parasite
detection laboratory methods in this patient
population.
Conflict of Interest: The author declares no
conflict of interest related to this article.
Funding sources: The author declares that this
study has received no financial support.
Ethics Committee Approval: Ethics committee
approval of the study was obtained from Hatay
Mustafa Kemal University Tayfur Ata Sökmen
Faculty of Medicine Clinical Research Ethics
Committee with the decision number 131, dated
17.11.2015.
Acknowledgement: I would like to thank Prof Dr
Özlem Makbule Kaya from Hatay Mustafa Kemal
University, Parasitology Department for doing
parasitology laboratory tests
Peer-review: Externally peer reviewed.
ORCID and Author contributions: MÖY (0000-
0001-8346-8941): Concept and design, materials,
data collection, literature search, statistical
analysis, writing, critical review.
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