CLINICAL SCIENCE
High Prevalence of Demodex Infestation is Associated With
Poor Blood Glucose Control in Type 2 Diabetes Mellitus: A
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Cross-Sectional Study in the Guangzhou Diabetic Eye Study
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Nuan Zhang, MD, Kuiyao Wen, MD, Yan Liu, MD, Wenyong Huang, MD, PhD,
Xiaoling Liang, MD, PhD, and Lingyi Liang, MD, PhD
Purpose: The aim of this study was to investigate the association
between type 2 diabetes mellitus (T2DM) and ocular Demodex
mite infection.
Method: About 381 patients with T2DM from nearby communities
were enrolled, and 163 age-matched and sex-matched nondiabetic
patients from the cataract clinic were included as the control group.
All subjects underwent personal history and demographic data
collection, ocular examination, and lash sampling, followed by
microscopic identification and counting of Demodex mites. Binoc-
ular fundus photography was performed for diabetic patients.
Statistical correlation between ocular Demodex infestation and
T2DM and blood glucose control status was performed.
Results: The Demodex mite infestation rate (62.5% vs. 44.8%,
P , 0.001) and count [3 (0–12) vs. 2 (0–9.6), P = 0.01], especially
of Demodex brevis (18.9% vs. 4.9%, P , 0.001) [0 (0–1) vs.
0 (0–0), P , 0.001], were significantly higher in the T2DM patient
group than that in the control group. The ratio of Demodex brevis to
Demodex folliculorum in the T2DM patient group was significantly
higher than that in the control group (1:3 vs. 1:9, P , 0.001).
Diabetic patients presented with more cylindrical dandruff (55.1%
vs. 39.3%, P = 0.001). Ocular Demodex infestation was strongly
associated with poor blood glucose control (HbA1c . 7%) (odds
ratio = 1.82; 95% confidence interval, 1.12–2.94; P = 0.2) and
female sex (odds ratio = 1.69, 95% confidence interval, 1.08–2.65,
P = 0.02). No association was found between Demodex infestation
and the severity of diabetic retinopathy.
Received for publication February 1, 2022; revision received June 14, 2022;
accepted June 28, 2022. Published online ahead of print December 12,
2022.
From the State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic
Center, Sun Yat-sen University, Guangdong Provincial Key Laboratory of
Ophthalmology and Visual Science, Guangzhou, China.
Supported by the National Natural Science Foundation of China (81770892
and 81300739), the Guangdong Natural Science Foundation
(2019A1515012012), and the grant from the High-level Hospital
Construction Project of Guangdong Province (303020101).
The authors have no conflicts of interest to disclose.
N. Zhang and K. Wen contributed equally to the work presented and, as such,
are regarded as co-first authors.
Correspondence: Lingyi Liang, MD, PhD, State Key Laboratory of
Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University,
54S Xianlie Nan Rd, Guangzhou 510060 (e-mail: lingyiliang@qq.com).
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Conclusions: Patients with T2DM, especially those with poor
blood glucose control, tend to have a higher prevalence of ocular
Demodex infestation, suggesting that high blood glucose is a risk
factor for demodicosis.
Key Words: Demodex, T2DM, blood glucose control
(Cornea 2023;42:670–674)
D emodex is one of the most common parasites living in
mammals.1 Among the many species, only Demodex
folliculorum and Demodex brevis are found in humans,
infecting the face, cheek, forehead, nose, ear canal, and
eyelid.2–4 On the eyelids, the longer D. folliculorum parasit-
izes the roots of the eyelashes and hair follicles, whereas the
shorter D. brevis parasitizes the deep part of the sebaceous
glands and meibomian glands. The infection rate of Demodex
varies among different studies, ranging from 20% to 70%,1 of
which D. folliculorum is the main species. In healthy people,
the ratio of D. folliculorum to D. brevis is approximately 10:1,
but in those with eye diseases, D. brevis infection is greatly
increased.5–7 Therefore, D. brevis is considered to have
stronger pathogenicity. Although it can be detected in healthy
people, the increased number of Demodex is considered to be
related to ocular surface changes, such as typical cylindrical
dandruff (CD), lash disorders, blepharitis, meibomian gland
dysfunction, dry eye, keratitis, keratoconjunctivitis, chala-
zion, and the recurrence of pterygium.1,8–10
A variety of risk factors have been reported to be
associated with ocular Demodex infection, such as age,
immunosuppression, poor personal hygiene, wearing glasses,
obesity, oily skin, malnutrition, and skin disorders, such as
rosacea, etc.11,12 In recent years, type 2 diabetes mellitus
(T2DM) has been considered to be linked with systemic
immune and metabolic disorders.13,14 Diabetic patients have
increased rates of meibomian gland dysfunction, dry eye,
persistent corneal epithelial defects, etc.15 In the literature, an
association between diabetes mellitus (DM) and ocular
Demodex infestation has been reported by 2 small sample
size studies including 28 patients with DM and 33 patients
with gestational DM.16,17 However, it remains less known
whether such an increased risk of ocular Demodex infestation
is correlated with blood glucose control and with the ocular
complications of DM, such as diabetic retinopathy
(DR).16,18,19
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 Cornea
Volume 42, Number 6, June 2023
To address these questions, we conducted a prospec-
tive, comparative study to investigate the prevalence of
Demodex mite infestation in patients with and without
T2DM. The plausible risk factors for ocular Demodex
infestation in these patients were further analyzed.
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METHODS
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Population
This study followed the principles of the Declaration of
Helsinki and was approved by the Ethics Committee of the
Zhongshan Ophthalmic Center (Guangzhou, China)
(2017KYPJ094). The study recruited 381 patients with
T2DM, aged older than 45 year, from the nearby communities
from November 2017 to April 2019 in the “Guangzhou Diabetic
Eye Disease Research” project. The control group enrolled 163
age-matched and sex-matched nondiabetic patients from the
cataract clinic at the Zhongshan Ophthalmic Center.
Patients with systemic diseases other than T2DM, those
with other ocular infectious or inflammatory diseases, those
with a history of eye surgery or trauma within 6 months
before enrollment, and those who could not cooperate with
the examination were excluded. Patients were informed on
the methods of the study, particularly on the removal of
eyelashes, and informed consent was obtained from
each subject.
Data Collection and Ocular Examination
Patient demographic information, including name, age,
sex, height, and weight, was obtained. Body mass index
(BMI) was calculated. A slit-lamp microscope (Topcon,
Japan) was used to observe the condition of the eyelids,
eyelashes, and conjunctiva. DR was graded according to the
International Clinical Diabetic Retinopathy Disease Severity
Scale (2002) from the American Academic of Ophthalmology
by fundus images taken by a CR-2 fundus camera (Canon,
Japan) in all patients with T2DM. Patients without DR in both
eyes were included in the without DR group, patients
diagnosed with nonproliferative DR (NPDR) in both eyes
were included in the NPDR group, and patients diagnosed
with proliferative diabetic retinopathy (PDR) in either eye
were included in the PDR group.
Eyelash Sampling and Counting of Demodex
by Microscopy
According to previous studies,5 eyelash sampling and
Demodex microscopic examination were performed. In
short, 3 eyelashes with typical CD, which is considered
pathognomonic for Demodex infestation, were previously
selected; otherwise, 3 lateral, middle, and medial lashes
were removed from each eyelid and observed under a slit-
lamp microscope (Nikon, Japan). The distinction of the 2
species was made according to the shape of Demodex mites
(Fig. 1). Demodex infection was defined as the detection of
3 or more Demodex mites in 12 eyelashes, D. folliculorum
infection was defined as 3 or more D. folliculorum in 12
eyelashes, and D. brevis infection was defined as 1 or more
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Prevalence of Demodex Infestation
D. brevis in 12 eyelashes because D. brevis is less common
in normal healthy people.
Blood Glucose Level
Blood glucose status was defined according to the level
of glycosylated hemoglobin (HbA1c) in the venous blood.
Fasting venous blood was collected from patients with
T2DM. According to the “Standards of Medical Care in
Diabetes (2020)” issued by the American Diabetes Associa-
tion,20 patients with an HbA1c level .7% were included in
the poorly controlled blood glucose group and those with an
HbA1c level #7% were included in the well-controlled blood
glucose group.
Statistical Analysis
Descriptive statistics are reported as mean 6 SD for
normally distributed variables and the median (P10–P90) for
abnormally distributed continuous variables. The independent
samples t test and Mann–Whitney U test were used to
determine age matching and the Demodex count between the
2 groups, whereas the ANOVA test and the Kruskal–Wallis H
test were used among the 3 groups. The Pearson x2 test was
used for the rest of the comparative and correlation analyses,
and the Z test was used to compare ratios. A binary logistic
regression analysis was performed to evaluate the risk factors
for Demodex infestation in diabetic patients. All statistical
analyses were performed using SPSS software version 26.0
(SPSS, Inc, Chicago, IL) and were reported as 2-tailed
probabilities, with P , 0.05 considered significant.
RESULTS
A total of 381 patients with T2DM were included in the
diabetic group, including 154 (59.6%) men and 227 (40.4%)
women, with an average age of 65.7 6 8.6 (45–86) years. The
control group included 163 individuals without diabetes,
including 57 men (35.0%) and 106 women (65.0%), with an
average age of 67.0 6 6.8 (50–82) years. The two groups
were matched by age and sex (P = 0.09 and P = 0.23). The
average BMI of the diabetic group was 24.6 6 3.3, whereas
that of the control group was 23.4 6 3.2, with that of the
diabetic group being significantly higher (P , 0.001)
(Table 1).
The infestation rate of Demodex in the diabetic group
was 62.5% of the 381 patients, which was significantly higher
than that of the control group, which was 44.8% of the 163
patients (P , 0.001). The median count was also significantly
higher in the diabetic group [3 (0–12) vs. 2 (0–9.6), P = 0.01].
When considering the 2 species separately, the infestation
rates of D. brevis and D. folliculorum in the diabetic group
were 18.9% and 57.7%, respectively, which were greater than
those in the control group (4.9% and 44.8%, P , 0.001,
P = 0.01). The ratio between D. brevis and D. folliculorum
was 1:3 in the diabetic group and 1:9 in the control group
(P , 0.001). The median count of Demodex was higher in the
diabetic patients, regardless of whether the species was D.
brevis or D. folliculorum [0 (0–1) vs. 0 (0–0), P , 0.001 and
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 Zhang et al Cornea
Volume 42, Number 6, June 2023
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FIGURE 1. Image of A, D. folli-

culorum and B. D. brevis. (The full
color version of this figure is avail-
able at www.corneajrnl.com.)

3 (0–12) vs. 2 (0–9.6), P = 0.03, respectively] (Table 1). 66.5 6 8.4 years, P = 0.02), but there was no significant
Patients with T2DM were not more likely to have conjunc- sex difference (male:female = 45.8%:54.2% vs.
tival congestion or meibomian gland abnormalities (23.9% 37.6%:62.4%, P = 0.12). In addition, the average BMI in
vs. 22.7%, 92.1% vs. 90.8%, respectively, both P . 0.05). the poorly controlled subgroup was significantly higher
However, CD, the characteristic sign of Demodex infection, (25.2 6 3.2 24.4 6 3.4, P = 0.03). The Demodex
was more common in patients with T2DM (55.1% vs. 39.3%, infestation rate (71.0% vs. 58.0%, P = 0.01) and count
P = 0.001) (Table 1). [5 (0–14.6) vs. 3 (0–11.9), P = 0.02] in patients with poor
To investigate whether the severity of diabetes is control were significantly higher than those in patients with
associated with ocular Demodex infestation, we correlated good control. Considering the two species, the D. brevis
the HbA1c level of patients with diabetes and ocular Demodex infestation rate (25.2% vs. 15.6%, P = 0.02) and count
infestation. Among the patients with diabetes, 131 of 381 [0 (0–2) vs. 0 (0–1), P = 0.02] and the D. folliculorum
people (34.4%) had poorly controlled HbA1c (HbA1c .7%), infestation rate (64.9% vs. 54.0%, P = 0.04) and count
and 250 patients (65.6%) had well-controlled HbA1c [4 (0–13) vs. 3 (0–11), P = 0.03] were all significantly
(HbA1c #7%). The average age of the patients in the poorly higher in the poorly controlled subgroup. In addition, the
controlled subgroup was significantly younger (64.2 6 8.6 vs. ratio of the infestation rate of D. brevis to D. folliculorum
was 1:3, which was slightly higher than that in the well-
controlled subgroup (1:4, P = 0.09) (Table 2).
TABLE 1. Demodex Infestation in Diabetic and Nondiabetic
Patients Diabetic retinopathy is one of the indices used to
evaluate the severity of diabetes; therefore, we grouped
Diabetes Control
(n = 381) (n = 163) P
diabetic patients into the without DR, NPDR, and PDR
subgroups. The incidence rate of DR was 25.5% (97/381) in
Age (yr), mean 6 SD 65.7 6 8.6 67.0 6 6.8 0.09
our study, of which 23.1% (88/381) of the patients had NPDR
Sex, male, n (%) 154 (59.6) 57 (35.0) 0.23*
and 2.4% (9/381) had PDR. Age and BMI were comparable
BMI (kg/m2), mean 6 SD 24.6 6 3.3 23.4 6 3.2 ,0.001
among the 3 subgroups, but male sex was more in the PDR
Diabetes duration (yr), 9.7 6 7.9 — —
mean 6 SD
group (37.0% vs. 47.7% vs. 77.8%, P = 0.01). There were no
Demodex infestation, n (%) 238 (62.5) 73 (44.8) ,0.001*
significant differences in infestation rates and counts for total
Counts of Demodex, 3 (0–12) 2 (0–9.6) 0.01†
Demodex species or for D. folliculorum (all P . 0.05). In the
median (P10–P90) PDR group, no patient with D. brevis infestation was
D. brevis infestation, n (%) 72 (18.9) 8 (4.9) ,0.001* detected, and the infestation rates were similar in the other
Counts of D. brevis, 0 (0–1) 0 (0–0) ,0.001† 2 subgroups (P . 0.05) (Table 2). We also analyzed the
median (P10–P90) difference between patients with and without DR, which was
D. folliculorum infestation, n (%) 220 (57.7) 73 (44.8) 0.01* similar to the above results.
Counts of D. folliculorum, 3 (0–12) 2 (0–9.6) 0.03† To investigate risk factors between diabetes and ocular
median (P10–P90) Demodex infestation, binary logistic regression analysis was
D. brevis:D. folliculorum 1:3 1:9 ,0.001‡ performed. The results showed that women were 1.69 times
Conjunctival congestion，n (%) 91 (23.9) 37 (22.7) 0.77* more likely to have ocular Demodex infestation [odds ratio
CD，n (%) 210 (55.1) 64 (39.3) 0.001* 1.69 (95% confidence interval 1.08–2.65), P = 0.02] and
Meibomian gland abnormalities, 351 (92.1) 148 (90.8) 0.61* those with poor HbA1c control were 1.82 times more
n (%) susceptible to Demodex infestation [odds ratio 1.82 (95%
The Student t test was used in the table except additional mentioned. confidence interval 1.12–2.94), P = 0.02]. However, in
*Pearson x2 test. patients with T2DM, age, BMI, diabetes duration, and DR
†Mann–Whitney U test.
‡Z test. status were not related to ocular Demodex infection (all
P . 0.05) (Table 3).

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 Cornea
Volume 42, Number 6, June 2023 Prevalence of Demodex Infestation

TABLE 2. Demodex Infestation in Diabetic Population

HbA1c .7% HbA1c #7% Without DR NPDR
(n = 131) (n = 250) P (n = 284) (n = 88) PDR (n = 9) P
Age (yr), mean 6 SD 64.2 6 8.6 66.5 6 8.4 0.02 66.0 6 8.7 65.2 6 7.9 61.33 6 10.01 0.22*
Sex, male, n (%) 60 (45.8) 94 (37.6) 0.12† 105 (37.0) 42 (47.7) 7 (77.8) 0.01†
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BMI (kg/m2), mean 6 SD 25.2 6 3.2 24.4 6 3.4 0.03 24.7 6 3.3 24.4 6 3.5 25.7 6 3.0 0.44*
Demodex cases, n (%) 93 (71.0) 145 (58.0) 0.01† 173 (60.9) 60 (68.2) 5 (55.6) 0.43†
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Counts of Demodex, median (P10-P90) 5 (0–14.6) 3 (0–11.9) 0.02‡ 3 (0–12) 5 (0–16) 3 (1–10) 0.23§
D. brevis cases, n (%) 33 (25.2) 39 (15.6) 0.02† 53 (18.7) 19 (21.6) — 0.28†
Counts of D. brevis, median (P10-P90） 0 (0–2) 0 (0–1) 0.02‡ 0 (0–1) 0 (0–2) — 0.26§
D. folliculorum cases, n (%) 85 (64.9) 135 (54.0) 0.04† 161 (56.7) 55 (62.5) 5 (55.6) 0.59†
Counts of D. folliculorum, median 4 (0–13) 3 (0–11) 0.03‡ 3 (0–12) 5 (0–14.2) 3 (1–10) 0.30§
（P10-P90）
D. brevis: D. folliculorum 1:3 1:4 0.09k 1:3 1:3 — 0.39k
The Student t test was used in the table except additional mentioned.
*ANOVA test.
†Pearson chi-squared test
‡Mann–Whitney U test.
§Kruskal–Wallis H test.
kZ test.

DISCUSSION previous studies. A possible reason is that our patients were

This study is the first population-based cross-sectional relatively elderly, and the infection rate is known to increase
study to investigate ocular Demodex infection in patients with with age.21
T2DM and found that the infection rate and count of Plausible reasons for the higher infection rate and
Demodex were significantly increased in patients with Demodex count in patients with T2DM are as follows: First,
T2DM. Poorly controlled HbA1c is a risk factor for ocular high glucose in the body may be beneficial to the growth and
Demodex infection, increasing the risk by 1.82 times, whereas metabolism of Demodex mites. We found that patients with
the severity of DR is not related to Demodex infection. poor HbA1c control had a higher infection rate and count,
Previous studies also reported a higher Demodex similar to those of patients with skin Demodex,19 and HbA1c
infection rate in diabetic patients. Clifford et al found that levels were related to Demodex infection. High glucose status
the infection rate of D. folliculorum in diabetic patients was may change the lipid metabolism of the meibomian glands
36%, which was higher than that in people without diabetes making it more suitable for Demodex to grow. Second,
(13.6%).17 Keskin Kurt et al16 focused on patients with diabetes-related immune abnormalities may be another
gestational DM and found that the infection rate of D. reason.22–28 The immune system in diabetic patients changes
folliculorum was 27.2%. The infection rate of Demodex in where Demodex is prone to colonize. Many studies have
our study was 62.5%, which was much higher than those in confirmed that immunocompromised patients are more sus-
ceptible to Demodex infection.29–31
The Demodex infestation rates increased with the
severity of DR, but there was no association between them.
TABLE 3. Risk Factors of Demodex Infestation in Diabetic This may be because the patients with T2DM we enrolled
Patients
were from the nearby communities and had mild symptoms.
OR (95% CI) P The innovation in our study lies in the inclusion of
Age (yr), mean 6 SD 1.03 (1, 1.05) 0.05 diabetic patients from nearby communities, who did not have
BMI (kg/m2) 0.96 (0.90, 1.02) 0.2 eye problems or undergo ocular surface treatment interven-
Diabetes duration(yr), mean (SD) 1.01 (0.98, 1.04) 0.5 tion. In this case, we can offer medical healthcare before the
Sex disease progresses. In addition, previous studies on the
Male Reference 0.02 association between ocular Demodex infestation and diabetes
Female 1.69 (1.08, 2.65) were all hospital-based, and Demodex infestation may be
HbA1c confounded by diseases other than diabetes. This concern is
HbA1c # 7% Reference 0.02 partly mitigated by our community-based study. Furthermore,
HbA1c . 7% 1.82 (1.12–2.94) our study is the first to report the correlation between ocular
DR Demodex infestation and the severity of DR, as well as blood
Without DR Reference glucose control.
NPDR 1.53 (0.38–6.14) 0.6 There are some limitations in our study: the sample size
PDR 1.70 (0.41, 7.01) 0.5 in the PDR group was small, and we did not enroll type 1
CI, confidence interval; OR, odds ratio. diabetes patients or the younger patients, which needs to be
improved on in further studies.

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 Zhang et al
In summary, our study is the first community-based
cross-sectional study showing that the infection rate and
count of Demodex in patients with T2DM were higher than
those in normal people. Poor blood sugar control is a risk
factor for ocular Demodex infection in these patients, which
stresses the importance of controlling blood glucose in
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