Journal of Ophthalmology

Journal of Ophthalmology / 2019 / Article
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Effects of Ageing on the Eye Structure and Function 2019

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Research Article | Open Access

Volume 2019 |Article ID 8949683 | https://doi.org/10.1155/2019/8949683

Jing Zhong, Yiwei Tan, Saiqun Li, Lulu Peng, Bowen Wang, Yuqing Deng, Jin Yuan, "The Prevalence of Demodex folliculorum and Demodex brevis in Cylindrical Dandruff Patients", Journal of Ophthalmology, vol. 2019, Article ID 8949683, 7 pages, 2019. https://doi.org/10.1155/2019/8949683

The Prevalence of Demodex folliculorum and Demodex brevis in Cylindrical Dandruff Patients

Academic Editor: Alejandro Cerviño
Received08 Nov 2018
Revised03 Feb 2019
Accepted12 Mar 2019
Published03 Apr 2019

Abstract

Purpose. To compare the prevalence of and factors associated with Demodex brevis and Demodex folliculorum in patients with cylindrical dandruff (CD group) and healthy controls. Methods. Eyelashes were taken from 1680 patients with CD and 1700 healthy controls in China from March 2015 to May 2017. All patients underwent a complete eye examination, and Demodex spp. were counted. The prevalence was analyzed according to age, gender, and clinical features. Results. Mean patient age was 42.93 ± 16.52 (3–88) and 39.4 ± 13.6 (7–81) years old in the CD and healthy control groups, respectively. In the CD and healthy groups, the positive rate for Demodex folliculorum was 27.92% and 8.47%, respectively, while that for Demodex brevis was 31.67% and 6.65%, respectively. In the CD group, the prevalence of Demodex brevis was higher than that of Demodex folliculorum, no matter in the females (33.65% versus 29.01%) or the males (28.54% versus 23.88%) in the CD group. Moreover, the numbers of Demodex folliculorum and Demodex brevis were significantly and positively correlated with age, in both children and old patients (both ), as well as with the severity of eyelid congestion (all ). Conclusions. In a large sample population, the prevalence of Demodex brevis and Demodex folliculorum was higher in the CD group than in healthy volunteers. In addition, the severity of eyelid congestion might be exacerbated by the number of Demodex spp., which may therefore provide a good clinical reference and objective guide.

1. Introduction

Demodex, one of the most common parasites in humans, resides in sites with numerous hair follicles and pilosebaceous glands, such as the eyelids [1], face [2], scalp [3], and upper chest [4]. Among more than 140 species of mites, only Demodex folliculorum and Demodex brevis are found on the human body. Demodex folliculorum is approximately 0.3–0.4 mm long, while Demodex brevis is approximately 0.2–0.3 mm long [5]. Their life cycle is approximately 14–16 days long, they move mostly at night, and they live in regions such as the sebaceous glands in facial skin, including the nose, nasolabial folds, eyelids, cheek, forehead, chin, and neck [6].

In ophthalmology, ocular demodicosis is typically accompanied by eyelash loss or abnormal alignment and chronic inflammation of the meibomian gland [7], leading to lipid tear deficiency in the conjunctiva [8]; in turn, this deficiency leads to conjunctivitis and sight-threatening keratitis in the cornea [9]. Several studies have also linked the presence of Demodex with chronic blepharitis because the mite can perpetuate the follicular inflammatory process [1, 10, 11]. Some researchers consider the mites to be merely passengers on skin because they are found on almost all normal adult skin and thus are coincidentally found on diseased skin [12, 13]. However, clinical observations have revealed that after ineffective conventional therapy, acaricidal therapy can eliminate the clinical symptoms of blepharitis [14]. Nevertheless, direct, absolute proof of a causal relationship has not yet been established because Demodex is a host-specific obligate parasite that currently cannot be cultured in vitro to parasitize and infect other animal hosts [15]. Therefore, clinical observations based on large samples are important for exploring the relationship between Demodex and clinical signs.

Cylindrical dandruff (CD) in the eyelashes, also known as cylindrical casts, are scales that form clear cuffs that collar the lash root and may be composed of keratins and lipids [16, 17]. CD is one of the clinical manifestations of ocular demodicosis, and Tseng’s study showed that eyelashes with CD did indeed have a significantly higher rate of Demodex infestation than was found in eyelashes without CD [6]. CD in the eyelashes is a common finding in some patients with ocular demodicosis, but whether it is pathognomonic of Demodex infestation remains controversial. This debate is partially attributed to the accuracy of methods used to sample and count Demodex [18]. Therefore, a modified sampling and counting method was established to enhance the accuracy of Demodex diagnosis [6].

However, the exact prevalence of Demodex and the pathogenic potential of these mites in eyes with CD remain uncertain. Thus, we performed a study of 1680 patients with CD and 1700 healthy volunteers in China that was designed to determine the prevalence of Demodex and the effect of the hosts’ factors such as gender, age, and eyelid inflammation score, on the presence or absence of Demodex.

2. Materials and Methods

2.1. Patient Data

A total of 1680 patients with eyelashes showing CD (representative pictures are shown in Figure 1(a)) and who complained of ocular surface irritation and 1700 healthy volunteers who visited our hospital between March 2015 and June 2017 were included in our study. In the healthy group, there were 1166 (68.6%) females and 534 (31.4%) males with a mean age of 39.4 ± 13.6 (7–81) years; in the CD group, there were 1165 (69.4%) females and 515 (30.6%) males with a mean age of 42.9 ± 16.5 (3–88) years. The collected data included basic information such as gender and age, the status of eyelid inflammation, and the results of Demodex counting. This study followed the tenets of the Declaration of Helsinki and was approved by the Ethics Committee of the Zhongshan Ophthalmic Center (Guangzhou, China). A total of 3380 individuals in both groups all signed a consent document to participate in the study.

2.2. Demodex Sampling and Counting

The methods used here were previously described by Kheirkhah et al. [19]. Briefly, two lashes with CD were removed from each lid of each subject by fine forceps and were placed separately on each end of a glass slide for examination under a slit-lamp biomicroscope (SL220; Carl Zeiss, Oberkochen, Germany) at a magnification of ×25. Thus, for each subject, a total of 8 lashes were prepared on 4 slides. A coverslip was mounted on each lash before 20 μL of saline was slowly pipetted at the edge of the coverslip until it surrounded the lash. Then, 20 μL of 100% alcohol (Sigma-Aldrich, St. Louis, MO) was pipetted at the edge of the coverslip; this prolonged the counting time for up to 20 minutes and allowed the embedded Demodex to migrate from the CD. Under the microscope, the number of Demodex was counted three times, and all samples were photographed in a conventional manner by the same specialist (Doc Tan). The presence of Demodex in at least one of the 8 eyelashes was defined as Demodex-positive.

2.3. Eyelid Inflammation Evaluation

The status of eyelid inflammation was based on the presence of vascular congestion in the eyelid margin, as observed by external photography. These findings were subjectively rated on a four-point scale, as follows: 0, no vascular congestion; 1, mild vascular congestion; 2, moderate vascular congestion; and 3, severe vascular congestion [20].

2.4. Statistical Analysis

Data were evaluated using SPSS for Windows 11.5. An unpaired, two-tailed Student’s t-test was used to compare the numbers of Demodex brevis and Demodex folliculorum and the numbers of Demodex among the different grades of eyelid congestion. The chi-square test and Fisher’s exact test were used to evaluate differences in Demodex prevalence among different ages and genders. Correlation analysis was used to evaluate the relationship between Demodex numbers and age and between Demodex rates and eyelid congestion severity. The data were considered significant at .

3. Results

3.1. The Prevalence of Demodex Brevis and Demodex Folliculorum Was Higher in the CD Group than in the Healthy Group

Figures 1(b) and 1(c) show representative microscopic images of Demodex folliculorum and Demodex brevis. The positive rate of Demodex folliculorum was 27.92% and 8.47%, respectively, in the CD group and healthy group, and Demodex brevis’s prevalence was 31.67% and 6.65%, respectively, in these two groups (Figure 1(d)). Furthermore, the average number of Demodex folliculorum and Demodex brevis was 0.52 (0–18) and 0.86 (0–18) in the CD group, which was 0.06 (0–2) and 0.14 (0–2) in the healthy group; the average Demodex.spp. number of all the positive subjects was more in the CD group than in the healthy group, no matter in Demodex folliculorum (2.23 ± 0.07 versus 1.37 ± 0. 08, ) or in Demodex brevis (2.72 ± 0.07 versus 1.29 ± 0.13, ). Moreover, the average number of Demodex brevis was obviously greater than Demodex folliculorum in the CD group () while not in the healthy group (Figure 1(e)). Thus, the prevalence of Demodex folliculorum and Demodex brevis was higher in CD group compared with that in the healthy group, and the positive rate of Demodex brevis was greater than that of Demodex folliculorum in the CD group.

3.2. The Number of Demodex Brevis Was Higher in Females than in Males

In the CD group, the positive rate of Demodex folliculorum was 23.88% and 29.10%, respectively, in males and females, while in the healthy group, it was 7.49% and 8.83%, respectively, in males and females. The prevalence of Demodex brevis showed a trend similar to that of Demodex folliculorum, with the positive rate of 28.54% and 33.65% in males and females in the CD group and 5.05% and 7.55% in males and females in the healthy group. The prevalence of Demodex folliculorum and Demodex brevis were higher in the CD group than in the healthy group in both males and females and higher in females than in males in both groups (Figure 2).

3.3. The Number of Demodex Increased with Age in Eyelashes with CD

In the CD and healthy groups, the prevalence of Demodex folliculorum was 13.33% and 0% in children (<6 years old), 22.22% and 1.78% in juveniles (7–17 years old), 21.74% and 8.71% in youth (18–40 years old), 24.31% and 9.18% in middle-aged patients (41–65 years old), and 30.97% and 12.87% in old patients (66–88 years old) (Table 1). In the CD and healthy groups, the prevalence of Demodex brevis were 26.67% and 2.63% in children, 30.00% and 3.55% in juveniles, 29.55% and 6.46% in youth, 32.67% and 7.75% in middle-aged patients, and 37.42% and 8.77% in old patients. The prevalence of Demodex brevis and Demodex folliculorum appeared lower in younger age groups than in older age groups, respectively (Table 1). The prevalence differed among different groups, and old patients had the higher prevalence in Demodex folliculorum and Demodex brevis. Furthermore, in the CD group, the number of Demodex folliculorum and Demodex brevis per patient was positively correlated with age across all age groups (both ). The following equations were used: number of Demodex folliculorum = 1.180 + 0.035 (age) (r = 0.237, ) (Figure 3(a)) and number of Demodex brevis = 0.650 + 0.037 (age) (r = 0.286, ) (Figure 3(b)).


Age (years)Demodex folliculorum, positive/n (%)Demodex brevis, positive/n (%)
CD groupHealthy groupCD groupHealthy group

0–62/15 (13.33%)0/38 (0%)4/15 (26.67%)1/38 (2.63%)
7–1720/90 (22.22%)3/169 (1.78%)27/90 (30.00%)6/169 (3.55%)
18–40142/653 (21.74%)62/712 (8.71%)193/653 (29.55%)46/712 (6.46%)
41–65186/765 (24.31%)56/610 (9.18%)250/765 (32.67%)46/610 (7.75%)
66–8848/155 (30.97%)22/171 (12.87%)58/155 (37.42%)15/171 (8.77%)

3.4. The Prevalence and Number of Demodex Brevis Were Positively Correlated with the Severity of Eyelid Congestion

In the CD group, we concluded that the severity of eyelid congestion was positively correlated with the prevalence of both Demodex folliculorum and Demodex brevis (both ) (Figure 4(a)) according to the following equations: prevalence of Demodex folliculorum (%) = 18.25 + 10.19 (grade) (r = 0.999, ) and prevalence of Demodex brevis (%) = 13.40 + 8.75 (grade) (r = 1.000, ). The prevalence of Demodex folliculorum increased from 22.26% in Grade I to 30.66% in Grade II to 39.75% in Grade III, while the prevalence of Demodex brevis increased from 28.70% to 38.09% and 49.01% in Grade I, II, to Grade III, respectively. Furthermore, the highest numbers of Demodex folliculorum and Demodex brevis individuals were observed in Grade III cases, whereas the fewest were observed in the Grade I cases (all ) (Figure 4(b)). Specifically, the prevalence and number of Demodex folliculorum and Demodex brevis increased with the severity of eyelid congestion.

4. Discussion

Demodex is a parasite commonly observed on human skin [21], and some investigators have suggested that there is a symbiotic relationship between mites and humans that may even beneficial for the hosts because these mites ingest bacteria that can grow in the follicular canal [22, 23]. However, a growing body of evidence indicates that these mites may also act as pathogens in a number of skin diseases, such as rosacea [24], alopecia [25], and chronic blepharitis [11].

The prevalence of Demodex folliculorum and Demodex brevis was clearly higher in the CD group than in healthy volunteers in our study; although the positive rate of 27.92% and 31.67% was lower than the prevalence of 100% in Tseng’s study [6], it also provided strong evidence to support the high prevalence in CD lashes. The eye is surrounded by protruding body parts such as the nose, brow, and cheek; the eyelid is not as accessible as the face is to daily cleansing hygiene. Therefore, once a Demodex infestation is established in the face, it is likely to spread and flourish in the eyelids. Microabrasions caused by the mite’s claws can induce epithelial hyperplasia and reactive hyperkeratinization around the base of the lashes, forming CD [26], which is closely associated with Demodex infestation. In addition, differences in sample size and regions among studies have led to a lack of consistent results until now. For example, Wesolowska et al. [27] reported that the overall prevalence of Demodex spp. is 41% in Poland, a rate of positivity of 37.3% was reported for Demodex spp. in Turkish volunteers [28], and a prevalence rate of 21.2% was found in Shangqiu City of Henan Province [29], 36.3% in Tangshan [30], and 51.5% in inner Mongolia [31]. Thus, the difference in prevalence between our and Tseng’s results might be normal.

Moreover, we found that the prevalence of Demodex folliculorum and Demodex brevis was higher in females than in males. The prevalence of Demodex brevis was 33.65%, which is similar to the rate of 39.3% found in women in the Malatya province in Turkey [32] but lower than the prevalence of 100% reported in Tseng’s study [6]. However, the gender distribution of Demodex spp. in the present study was not in agreement with the results of Elston’s study [33], in which men were typically more heavily infested than women with Demodex. The application of exogenous lipids in cosmetics may also affect the growth of Demodex mites in females because females have lower androgen levels, and the meibomian gland is an androgen target organ. Therefore, females may be more susceptible to meibomian gland dysfunction, the resultant lipid insufficiency, and therefore Demodex spp. attack [34].

Demodex spp. are acquired shortly after birth during nursing and become more abundant during puberty [33]. In our study, the total number of Demodex folliculorum and Demodex brevis per patient was significantly correlated with increasing age from children to older patients, and their prevalence was significantly higher in older patients than in youths or children. Why do mites proliferate much more in older patients? Some of the physical barrier characteristics of an elderly person’s facial skin, such as increased skin pH [35], reduced skin surface hydration levels [36], and abnormal fatty acid composition [37], are conducive to mite proliferation. Additionally, in healthy skin, Demodex mites can cause host damage, so they may seize the opportunity to proliferate as immunity decreases or the host becomes immunocompromised [22]. Thus, the elderly, who have comparatively poor sanitary conditions and practices, abnormal skin barriers, and relatively compromised immunity, would be easily invaded by Demodex spp. Moreover, the prevalence of Demodex brevis was more common than Demodex folliculorum in the CD group and healthy subjects, which might be due to the fact that Demodex folliculorum resides in the lash follicle, whereas Demodex brevis burrows deep into the lash’s sebaceous gland and the meibomian gland [38]. Although some studies reported that Demodex folliculorum can be more easily isolated than Demodex brevis and thus the prevalence of Demodex folliculorum was higher compared with the Demodex brevis [39], we deduced that the tendency might be different in Demodex brevis-related or Demodex folliculorum-related ocular diseases, and Demodex brevis might be more common in the sebaceous gland- or meibomian gland-related diseases, such as Chalaza [6], while Demodex folliculorum was more commonly seen in lash follicle-related diseases, such as posterior blepharitis, or keratoconjunctivitis [38].

In addition to CD, eyelid margin inflammation is one of the main clinical manifestations of ocular demodicosis; thus, the severity of eyelid inflammation may indicate the prognosis [40]. The increased number and extrafollicular localization of mites enhance the probability of a hypersensitivity reaction, inflammation, and the secretion of inflammatory cytokines. Regardless of the prevalence or number of Demodex folliculorum and Demodex brevis, both were positively correlated with eyelid congestion severity; these results demonstrate that the Demodex spp. infestation may act as a pathogen in ocular pathologic features. This result is in agreement with Tseng’s results [41].

In conclusion, we explored a large sample population and found that the prevalence of Demodex brevis and Demodex folliculorum were higher in the CD group than in healthy volunteers. Our results demonstrate that in eyelashes with CD, the prevalence of Demodex brevis is higher than that of Demodex folliculorum. We also found that the number of Demodex spp. increases with age and that females are attacked more easily than males by Demodex spp. In patients with CD eyelashes, the severity of eyelid congestion was exacerbated by the prevalence and number of Demodex spp. Further studies should focus on the specific mechanism of Demodex spp. infection, build diagnostic criteria for eyelid demodicosis, and explore the relationship between Demodex spp. and ocular immunology to develop therapies against Demodex.

Data Availability

The datasets will be provided via a link if required after publication.

Conflicts of Interest

None of the authors has any proprietary interests or conflicts of interest related to this submission. None of the authors has any conflicts of interest to disclose.

Authors’ Contributions

Jing Zhong and Yiwei Tan contributed equally to this work.

Acknowledgments

This study was supported by grants from the National Natural Science Foundation of China to JY (81670826)

References

  1. M. Galea, R. Sharma, S. Srinivasan, and F. Roberts, “Demodex blepharitis mimicking eyelid sebaceous gland carcinoma,” Clinical & Experimental Ophthalmology, vol. 42, no. 2, pp. 208–210, 2014. View at: Publisher Site | Google Scholar
  2. M. M. Hom, K. M. Mastrota, and S. E. Schachter, “Demodex,” Optometry and Vision Science, vol. 90, no. 7, pp. e198–e205, 2013. View at: Publisher Site | Google Scholar
  3. W. Helou, E. Avitan-Hersh, and R. Bergman, “Demodex folliculitis of the scalp,” American Journal of Dermatopathology, vol. 38, no. 9, pp. 658–663, 2016. View at: Publisher Site | Google Scholar
  4. Y. E. Zhao, L. P. Wu, Y. Peng, and H. Cheng, “Retrospective analysis of the association between Demodex infestation and rosacea,” Archives of Dermatology, vol. 146, pp. 896–902, 2010. View at: Publisher Site | Google Scholar
  5. A. Horváth, D. Neubrandt, Á. Ghidán, and K. Nagy, “Risk factors and prevalence of Demodex mites in young adults,” Acta Microbiologica et Immunologica Hungarica, vol. 58, no. 2, pp. 145–155, 2011. View at: Publisher Site | Google Scholar
  6. Y.-Y. Gao, M. A. Di Pascuale, W. Li et al., “High prevalence of Demodex in eyelashes with cylindrical dandruff,” Investigative Opthalmology & Visual Science, vol. 46, no. 9, pp. 3089–3094, 2005. View at: Publisher Site | Google Scholar
  7. K. G. Patel and V. K. Raju, “Ocular demodicosis,” West Virginia Medical Journal, vol. 109, pp. 16–18, 2013. View at: Google Scholar
  8. W. Chen and G. Plewig, “Human demodicosis: revisit and a proposed classification,” British Journal of Dermatology, vol. 170, no. 6, pp. 1219–1225, 2014. View at: Publisher Site | Google Scholar
  9. S. H. Lee, Y. S. Chun, J. H. Kim, E. S. Kim, and J. C. Kim, “The relationship between Demodex and ocular discomfort,” Investigative Opthalmology & Visual Science, vol. 51, no. 6, pp. 2906–2911, 2010. View at: Publisher Site | Google Scholar
  10. V. Bhandari and J. Reddy, “Blepharitis: always remember Demodex,” Middle East African journal of ophthalmology, vol. 21, no. 4, pp. 317–320, 2014. View at: Publisher Site | Google Scholar
  11. F. Laspina, M. Samudio, M. Arrúa et al., “Demodex spp. en pacientes con blefaritis crónica,” Revista Chilena de Infectología, vol. 32, no. 1, pp. 37–42, 2015. View at: Publisher Site | Google Scholar
  12. M. Kemal, Z. Sümer, M. I. Toker, H. Erdoğan, A. Topalkara, and M. Akbulut, “The prevalence of Demodex folliculorumin blepharitis patients and the normal population,” Ophthalmic Epidemiology, vol. 12, no. 4, pp. 287–290, 2005. View at: Publisher Site | Google Scholar
  13. S. Talghini, D. F. Fouladi, S. Babaeinejad, R. Shenasi, and S. M. Samani, “Demodex mite, rosacea and skin melanoma; coincidence or association?” Turkish Journal of Parasitology, vol. 39, no. 1, pp. 41–46, 2015. View at: Publisher Site | Google Scholar
  14. M. Türk, I. Oztürk, A. G. Sener, S. Küçükbay, I. Afşar, and A. Maden, “Comparison of incidence of Demodex folliculorum on the eyelash follicule in normal people and blepharitis patients,” Turkiye Parazitol Dergisi, vol. 31, pp. 296-297, 2007. View at: Google Scholar
  15. F. Forton, M.-A. Germaux, T. Brasseur et al., “Demodicosis and rosacea: epidemiology and significance in daily dermatologic practice,” Journal of the American Academy of Dermatology, vol. 52, no. 1, pp. 74–87, 2005. View at: Publisher Site | Google Scholar
  16. F. P. English, “Demodex folliculorum and oedema of the eyelash,” British Journal of Ophthalmology, vol. 55, no. 11, pp. 742–746, 1971. View at: Publisher Site | Google Scholar
  17. D. I. Kosik-Bogacka, N. Łanocha, A. Łanocha et al., “Demodex folliculorum and Demodex brevisin healthy and immunocompromised patients,” Ophthalmic Epidemiology, vol. 20, no. 3, pp. 159–163, 2013. View at: Publisher Site | Google Scholar
  18. A. M. S. Cheng, H. Sheha, and S. C. G. Tseng, “Recent advances on ocular Demodex infestation,” Current Opinion in Ophthalmology, vol. 26, no. 4, pp. 295–300, 2015. View at: Publisher Site | Google Scholar
  19. A. Kheirkhah, G. Blanco, V. Casas, and S. C. G. Tseng, “Fluorescein dye improves microscopic evaluation and counting of Demodex in blepharitis with cylindrical dandruff,” Cornea, vol. 26, no. 6, pp. 697–700, 2007. View at: Publisher Site | Google Scholar
  20. N. K. Kuscu, A. B. Toprak, S. Vatansever, F. M. Koyuncu, and C. Guler, “Tear function changes of postmenopausal women in response to hormone replacement therapy,” Maturitas, vol. 44, no. 1, pp. 63–68, 2003. View at: Publisher Site | Google Scholar
  21. A. Ozer, U. Karaman, S. Degerli, C. Colak, M. Karadan, and E. Karci, “Investigation of Demodex Spp. prevalence among managers and workers of health hazard bearing and sanitary establishment,” Journal of the Formosan Medical Association, vol. 111, no. 1, pp. 30–33, 2012. View at: Publisher Site | Google Scholar
  22. N. Lacey, S. Ní Raghallaigh, and F. C. Powell, “Demodex mites—commensals, parasites or mutualistic organisms?” Dermatology, vol. 222, no. 2, pp. 128–130, 2011. View at: Publisher Site | Google Scholar
  23. K. Fischer and S. Walton, “Parasitic mites of medical and veterinary importance—is there a common research agenda?” International Journal for Parasitology, vol. 44, no. 12, pp. 955–967, 2014. View at: Publisher Site | Google Scholar
  24. W. Chen and G. Plewig, “Are Demodex mites principal, conspirator, accomplice, witness or bystander in the cause of rosacea?” American Journal of Clinical Dermatology, vol. 16, no. 16, pp. 67–72, 2015. View at: Publisher Site | Google Scholar
  25. S. F. Li, X. T. Zhang, S. L Qi et al., “Allergy to dust mites may contribute to early onset and severity of alopecia areata,” Clinical and Experimental Dermatology, vol. 40, no. 2, pp. 171–176, 2015. View at: Publisher Site | Google Scholar
  26. C. L. Bevins and F. T. Liu, “Rosacea: skin innate immunity gone awry?” Nature Medicine, vol. 13, no. 8, pp. 904–906, 2007. View at: Publisher Site | Google Scholar
  27. M. Wesolowska, B. Knysz, A Reich et al., “Prevalence of Demodex spp. in eyelash follicles in different populations,” Archives of Medical Science, vol. 2, pp. 319–324, 2014. View at: Publisher Site | Google Scholar
  28. U. Karaman, Z. Koloren, O. Enginyurt, and A. Ozer, “The epidemiology of Demodex mites at the college students living in dormitories in the city of Ordu,” Turkish Journal of Parasitology, vol. 38, no. 3, pp. 166–171, 2014. View at: Publisher Site | Google Scholar
  29. J. H. Cui and C. Wang, “Facial Demodex infestation among urban and rural residents in Shangqiu city of Henan province,” Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, vol. 30, no. 4, pp. 283–285, 2012. View at: Google Scholar
  30. Y. S. Cao, Q. X. You, L Wang et al., “Facial Demodex infection among college students in Tangshan,” Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, vol. 27, no. 3, pp. 271–273, 2009. View at: Google Scholar
  31. Q. Hu and Y. Wang, “Investigation on the prevalence of human Demodex among 2,248 medical students in inner Mongolia,” Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, vol. 19, no. 4, pp. 239-240, 2001. View at: Google Scholar
  32. O. Enginyurt, U. Karaman, F. Cetin, and A. Ozer, “The prevalence of Demodex species and its relationship with the metabolic syndrome in women of Malatya province, Turkey,” Jundishapur Journal of Microbiology, vol. 8, no. 10, Article ID e24322, 2015. View at: Publisher Site | Google Scholar
  33. C. A. Elston and D. M. Elston, “Demodex mites,” Clinics in Dermatology, vol. 32, no. 6, pp. 739–743, 2014. View at: Publisher Site | Google Scholar
  34. D. A. Sullivan, B. D. Sullivan, J. E Evans et al., “Androgen deficiency, meibomian gland dysfunction, and evaporative dry eye,” Annals of the New York Academy of Sciences, vol. 966, no. 1, pp. 211–222, 2002. View at: Publisher Site | Google Scholar
  35. C. Gokce, O. Aycan-Kaya, E Yula et al., “The effect of blood glucose regulation on the presence of opportunistic Demodex folliculorum mites in patients with type 2 diabetes mellitus,” Journal of International Medical Research, vol. 41, no. 5, pp. 1752–1758, 2013. View at: Publisher Site | Google Scholar
  36. T. Yoshikawa and H. Kanazawa, “Association of plasma adiponectin levels with cellular hydration state measured using bioelectrical impedance analysis in patients with COPD,” International Journal of Chronic Obstructive Pulmonary Disease, vol. 7, pp. 515–521, 2012. View at: Publisher Site | Google Scholar
  37. S. Ni Raghallaigh, K. Bender, N. Lacey, L. Brennan, and F. C. Powell, “The fatty acid profile of the skin surface lipid layer in papulopustular rosacea,” British Journal of Dermatology, vol. 166, no. 2, pp. 279–287, 2012. View at: Publisher Site | Google Scholar
  38. J. Liu, H. Sheha, and S. C. Tseng, “Pathogenic role of Demodex mites in blepharitis,” Current Opinion in Allergy and Clinical Immunology, vol. 10, no. 5, pp. 505–510, 2010. View at: Publisher Site | Google Scholar
  39. E. Zeytun and Y. Karakurt, “Prevalence and load of Demodex folliculorum and Demodex brevis (Acari: Demodicidae) in patients with chronic blepharitis in the province of Erzincan, Turkey,” Journal of medical entomology, vol. 56, no. 1, pp. 2–9, 2019. View at: Publisher Site | Google Scholar
  40. S. L. Maskin, “Intraductal meibomian gland probing relieves symptoms of obstructive meibomian gland dysfunction,” Cornea, vol. 29, no. 10, pp. 1145–1152, 2010. View at: Publisher Site | Google Scholar
  41. A. Kheirkhah, V. Casas, W. Li, V. K. Raju, and S. C. Tseng, “Corneal manifestations of ocular Demodex infestation,” American Journal of Ophthalmology, vol. 143, no. 5, pp. 743–749, 2007. View at: Publisher Site | Google Scholar

Copyright © 2019 Jing Zhong et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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