Abstract
AimThe study aims to investigate the incidence and infestation of Demodex folliculorum in patients with gynecological cancer.MethodsThis cross-sectional study was carried out at Reyhanlı MMT Amerikan Hospital, Hatay, Turkey. Forty patients with gynecological cancer and 40 control subjects were included in the study. The age, presence of diabetes mellitus, body mass index (BMI), cancer type of individuals, and treatment method for cancer were recorded. A standardized skin surface biopsy method was used to determine if the patients had D. folliculorum infestation (>5 mites/cm² of skin).ResultsD. folliculorum was found to be positive in 14 (35.0%) of the patients with gynecological cancer and in 1 (2.5%) of the subjects in the control group. There was a significant difference between patient group and control group (p=0.001). There were no significant differences in age, presence of diabetes mellitus, chemotherapy and radiotherapy given or not, BMI between patients and control group. In cancer groups, particularly in ovarian cancer, density of D. folliculorum was found higher.ConclusionThe findings of this study suggest that immunosuppression states such as cancer increase the susceptibility to D. folliculorum mite infestation in patients with gynecological cancer.
Keywords
Introduction
Gynecological cancers, with incidence rates increasing annually, are a leading cause of death in women.1 There are many treatment modalities such as surgery, chemotherapy, and radiotherapy in the management of gynecological cancers. The presence of cancer as well as many treatment modalities cause immunosuppression via increasing some immunosuppressive cytokines and interleukins such as transforming growth factor-β (TGF-β) and interleukin-10 (IL-10).2 The immunosuppressive cytokines and interleukins (i.e., IL-10 and TGF-β) could cause development of parasitic infections in cancer patients.3-4
The human body, especially in immunosuppression state, contains many ectoparasites such as Demodex (D.) folliculorum and D. brevis. Ectoparasites might be present anywhere such as hair follicles, nasolabial folds, eyelids, cheeks, forehead, nose, and chin.5 Although many people are colonized by D. folliculorum, most of them remain asymptomatic. For that reason, some authors stated that D. folliculorum is an opportunistic pathogen. Furthermore, density of this opportunistic pathogen has been shown to be increased in immunosuppressive status such as leukemia, cancer, and AIDS (acquired immune deficiency syndrome).6
In the present study, we aimed to investigate incidence and infestation of D. folliculorum in patients with gynecologic cancers.
Materials and Methods
ParticipantsForty patients with gynecological cancer and 40 control subjects were included in the study. All examinations of patients were performed at Reyhanlı MMT Amerikan Hospital, Hatay, Turkey. Demographic (age and body mass index (BMI)) and clinical characteristics (cancer type, operation status, chemotherapy, radiotherapy, presence of diabetes mellitus, and skin type) of patients were obtained from clinical records. The patients were divided into three groups according to the cancer type: ovarian cancer group (OCG), endometrium cancer group (ECG), and cervix cancer group (CCG). Exclusion criteria were as follows: dermatitis related to Demodex species, previously diagnosed rosacea and facial seborrheic dermatitis, blepharitis, allergic disease, and the use of local or systemic antibiotics within the last two weeks.MethodsStandardized skin surface biopsy (SSSB) technique was used to evaluate the presence of D. folliculorum. Eyelashes and skin samples taken from cheek, chin, forehead, and nose were collected with SSSB technique from patients.7 The presence of D. folliculorum mites was investigated to determine the density of Demodex mites. A drop of cyanoacrylate-glue adhesive was put on a slide and the adhesive-carrying surface of the slide was applied to skin after wiping the patients’ face with alcohol. The slide was removed after one minute from the surface. A light microscope (Olympus CH20; Olympus Optical, Tokyo, Japan) at 40x and 100x magnifications was used to determine the density of D. folliculorum mites. The identification of >5 mites/cm² of skin was defined as a D. folliculorum mite infestation (Fig.1). The clinical examination, SSSB, and microscopy were done by the same clinician.Ethical ApprovalThe study was approved by the Ethics Committee of Adana City Education and Research Hospital (Date: 30.05.2024, Decision No: 3).Statistical AnalysisThe statistical analysis was performed using the Statistical Package for Social Sciences version 21 for Windows (SPSS Inc., Chicago, IL, USA). The Pearson Chi-square (χ²) test was performed to compare the prevalence of mites in the patient groups. The Student T test was used to evaluate the ages of patients. Local statistical significance was considered to be a p value less than 0.05 for all parameters.Reporting GuidelinesThis study was reported according to the STROBE guidelines.
Results
The mean age of patients with gynecologic cancer was 50.35 ± 9.72 and ranged between 40–72 years. In the control group, the mean age was 53.85 ± 5.23 and ranged between 42–67 years. The difference in age was not statistically significant (p˃0.05). BMI mean values of patients with gynecologic cancer and control group were 25.72 ± 2.36 and 24.83 ± 3.38, respectively. There was no statistical difference (p˃0.05).
In the current study, while 14 patients (35.0%) had D. folliculorum, one patient of the control group had D. folliculorum. There was a significant difference in the patient group and the control group (p=0.001). D. folliculorum infestation was positive in 9 (45.0%) of OCG patients, 4 (26.6%) of ECG patients, and 1 (20.0%) of CCG patients. The high rate of D. folliculorum in OCG and ECG was observed. There was no significant difference in the infestation of D. folliculorum according to the cancer type (p=0.172).
The rate of presence of diabetes mellitus in patients with gynecologic cancer was 52.5% and in the control group was 48.8%. The difference in incidence of diabetes mellitus was not statistically significant between the patient and the control group (p˃0.05). There was significant relation between patients with diabetes mellitus and D. folliculorum (p=0.052).
In the patient group with gynecologic cancer, 36 of 40 cases underwent operation (90.2%) and there was no significant association with D. folliculorum according to whether the operation was performed or not (p=0.756). Additionally, the rate of D. folliculorum was not significantly different in patients to whom chemotherapy and radiotherapy were given or not (p=0.15, 0.48, respectively).
The density of D. folliculorum (34.6%) was found more in eyelashes of patients with gynecologic cancer than skin area.
Discussion
Our study results revealed that patients with gynecological cancers had increased density of D. folliculorum when compared to the control group. As far as we know, this is the first study to investigate association between D. folliculorum infestations and gynecologic cancers.
There are few studies which investigated relationship between D. folliculorum and premalign lesions and cancers.8 Sonmez et al. showed increased D. folliculorum infestations in various cancer types especially breast cancer.9 Inci et al. found a high density of D. folliculorum in urological cancer.10 Erbagci et al. reported the high incidence of D. folliculorum infestations in eyelid basal cell carcinomas.11 In addition, hematological malignancies and non-melanoma skin cancer were found to be associated with higher density of D. folliculorum.12-13 Those studies suggested that immunosuppression plays a major role for increased density of D. folliculorum in eyelashes and skin.
Accordingly, in the current study, we found a high incidence of D. folliculorum infestation in patients with gynecological cancer which might also be related to the immunosuppression state. In our study, the incidence of D. folliculorum infestation in OCG was higher than in other gynecologic cancers. That might be the result of further immunosuppression seen in ovarian cancers. There are some studies which investigated the relationship between ovarian cancer and serum TGF-β and IL-10 levels.14-16 Therefore, high incidence of D. folliculorum infestation in OCG in our study might be related to these further immunosuppression states in ovarian cancers.
There are some predisposing factors related to increased D. folliculorum infestation such as old age, immunosuppressive status, AIDS, systemic or local corticosteroid usage, and diabetes mellitus.17-18 Aycan et al. reported that old age increases the density of D. folliculorum.17 However, in our study the mean age of patients and control groups was comparable. Gokce et al. showed the incidence of D. folliculorum is increased in diabetic patients at 24% in the study population.19 Besides, there were no significant differences between patient and control groups regarding diabetes. Although chemotherapy has immunosuppressive effects and leads to development of microbial infection, there were no differences in D. folliculorum infestation regarding whether chemotherapy was given or not in our study population. For that, we propose that gynecological cancers rather than chemotherapy might be related to increased D. folliculorum infestation.
Limitations
First, important limitation of the study was the small sample size. Second, we could not investigate D.folliculorum in other gynecological cancer types such as vaginal and tubal cancer.
Conclusion
We demonstrated a high density of D. folliculorum in patients with gynecological cancers. Moreover, D. folliculorum infestation was particularly increased in the ovarian cancer subtype. To reveal the exact pathogenesis of increased D. folliculorum infestation in gynecological cancers, further large scale studies should be carried out.
Declarations
Animal and Human Rights Statement
All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed Consent
Written informed consent was obtained from all patients.
Data Availability
The datasets used and/or analyzed during the current study are not publicly available due to patient privacy reasons but are available from the corresponding author on reasonable request.
Conflict of Interest
The authors declare that there is no conflict of interest.
Funding
None.
Abbreviations
BMI: Body mass index
ECG: Endometrium cancer group
OVG: Ovarian cancer group
SCG: Cervix cancer group
VCG: Vulva cancer group
References
- Maffione AM, Piva M, Tsamita CS, et al. Positron-emission tomography in gynecologic malignancies. Arch Gynecol Obstet. 2009;280:521-528. doi:10.1007/s00404-009-0979-2
- Yang L, Carbone DP. Tumor-host immune interactions and dendritic cell dysfunction. Adv Cancer Res. 2004;92:14-29. doi:10.1016/s0065-230x(04)92002-7
- Li MO, Wan YY, Sanjabi S, Robertson AKL, Flavell RA. Transforming growth factor β regulation of immune responses. Annu Rev Immunol. 2006;24:99-146. doi:10.1146/annurev.immunol.24.021605.090737
- Sabat R, Grütz G, Warszawska K, et al. Biology of interleukin 10. Cytokine Growth Factor Rev. 2010;21(5):331-344. doi:10.1016/j.cytogfr.2010.09.002
- Forton F, Germaux MA, Brasseur T, et al. Demodicosis and rosacea: epidemiology and significance in daily dermatologic practice. J Am Acad Dermatol. 2005;52(1):74-87. doi:10.1016/j.jaad.2004.05.034
- Damian D, Rogers M. Demodex infestation in a child with leukemia: treatment with ivermectin and permethrin. Int J Dermatol. 2003;42(9):724-726. doi:10.1046/j.1365-4362.2003.01916.x
- Aşkın Ü, Seçkin D. Comparison of the 2 techniques for measurement of the density of Demodex folliculorum: standardized skin surface biopsy and direct microscopic examination. Br J Dermatol. 2010;162(5):1124-1126. doi:10.1111/j.1365-2133.2010.09645.x
- Braathen L. 84th Annual Meeting of the Swiss Society for Dermatology and Venereology. Dermatology. 2002;205(3):308. doi:10.1159/000067150
- Sönmez Ö, Yalçın Z, Karakeçe E, Çiftci İ, Erdem T. Associations between Demodex species infestation and various types of cancer. Acta Parasitol. 2013;58(4):551-555. doi:10.2478/s11686-013-0178-y
- İnci M, Kaya ÖA, İnci M, et al. Investigating Demodex folliculorum in patients with urological cancer. Turkiye Parazitol Derg. 2012;36(4):208.
- Erbagci Z, Erbagci I, Erkiliç S. High incidence of demodicidosis in eyelid basal cell carcinomas. Int J Dermatol. 2003;42(7):567-571. doi:10.1046/j.1365-4362.2003.01928.x
- Karaman Ü, Şener S, Şamdancı E, Çolak C, Şaşmaz S. The incidence of Demodex species in skin biopsy specimens diagnosed as actinic keratosis and nonmelanoma skin cancer. Asian Biomed. 2010;4(2):343-348.
- Rabinovich A, Medina L, Piura B, Huleihel M. Expression of IL-10 in human normal and cancerous ovarian tissues and cells. Eur Cytokine Netw. 2010;21(2):122-128.
- Liu CZ, Zhang L, Chang XH, et al. Overexpression and immunosuppressive functions of transforming growth factor β1, vascular endothelial growth factor, and interleukin 10 in epithelial ovarian cancer. Chin J Cancer Res. 2012;24:130-137. doi:10.1007/s11670-012-0130-y
- Kulac M, Ciftci IH, Karaca S, Cetinkaya Z. Clinical importance of Demodex folliculorum in patients receiving phototherapy. Int J Dermatol. 2008;47(1):72-77. doi:10.1111/j.1365-4632.2007.03336.x
- Lau MT, So WK, Leung PC. Integrin β1 mediates epithelial growth factor-induced invasion in human ovarian cancer cells. Cancer Lett. 2012;320(2):198-204. doi:10.1016/j.canlet.2012.02.028
- Aycan Kaya Ö, Atambay M, Daldal N. Prevalence of Demodex folliculorum and Demodex brevis in the eyelashes of healthy subjects. Kafkas Univ Vet Fak Derg. 2012;18(suppl A):57-60.
- Lau GK. Hepatitis B reactivation after chemotherapy: 2 decades of clinical research. Hepatol Int. 2008;2(2):152-162. doi:10.1007/s12072-008-9056-3
- Gökçe C, Aycan-Kaya Ö, Yula E, et al. The effect of blood glucose regulation on the presence of opportunistic Demodex folliculorum mites in patients with type 2 diabetes mellitus. J Int Med Res. 2013;41(5):1752-1758. doi:10.1177/0300060513494730
Tables
Table 1. Distribution of D.folliculorum according to cancer type
D.F.: Demodex folliculorum, OVG; Ovarian cancer group, ECG; Endometrium cancer group, SCG; Cervix cancer group, VCG; Vulva cancer group
Table 2. Baseline clinical charecteristics of study population
BMI: Body mass index
Additional Information
Publisher’s Note
Bayrakol MP remains neutral with regard to jurisdictional and institutional claims.
Rights and Permissions
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0). To view a copy of the license, visit https://creativecommons.org/licenses/by-nc/4.0/
About This Article
How to Cite This Article
Atilla Karateke, Vicdan Köksaldı Motor. Demodex infestation in gynecologic cancers. Ann Clin Anal Med 2024;15(10):704-707. doi:10.4328/ACAM.22296
Publication History
- Received:
- 20.05.2024
- Accepted:
- 29.07.2024
- Published Online:
- 08.09.2024
- Printed:
- 01.10.2024