Evaluation of nasal and oropharyngeal flora in patients with acne vulgaris according to treatment options

Clinical trial Evaluation of nasal and oropharyngeal flora in patients with acne vulgaris according to treatment options Pınar Ozuguz1, MD, Elif E. C...
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Clinical trial

Evaluation of nasal and oropharyngeal flora in patients with acne vulgaris according to treatment options Pınar Ozuguz1, MD, Elif E. Callioglu2, MD, Kamil G. Tulaci2, MD, Seval D. Kacar1, MD, Ilknur Balta3, MD, Gulsah Asik4, MD, Serap Karatas1, MD, and Semsettin Karaca1, MD

1 Department of Dermatology, Faculty of Medicine, Afyon Kocatepe University, Afyon, 2Department of Otolaryngology, Etlik Educational and Research Hospital, Ankara, 3Dermatology, Kecioren Educational and Research Hospital, Ankara, and 4Department of Microbiology, Faculty of Medicine, Afyon Kocatepe University, Afyon, Turkey

Correspondence Pınar Ozuguz, MD Izmir Yolu 8 Km Afyon Turkey E-mail: [email protected] Conflicts of interest: None.

Abstract The aim of this study was to evaluate changes in nasal and oropharyngeal flora in patients with acne during treatments with tetracycline and isotretinoin. Swab specimens were taken from the right and left nasal cavities and oropharynx of 55 patients with acne and 20 healthy volunteers who were admitted to the dermatology department (Etlik Educational and Research Hospital, Ankara, Turkey) before the administration of treatment and in the third month of treatment. Study participants were divided into four groups as follows: patients with acne on topical treatment only, systemic isotretinoin, and systemic tetracycline, and the control group. Of 55 patients with acne, 18 were male and 37 were female. The mean age of the patients and the control group was 22.21  4.22 and 21.95  7.64, respectively. Staphylococcus aureus was isolated from the nasal flora of five patients, normal flora was suppressed in the oropharyngeal cultures of seven patients, and normal flora grew in the cultures of the other 20 patients who were on tetracycline treatment. On the other hand, normal flora grew in the nasal and oropharyngeal cultures of all the patients who were on isotretinoin treatment. Treatment options and follow-up procedures for acne vulgaris may lead to the development of bacterial resistance and damage to flora. In particular, systemic tetracycline treatment leads to changes in flora of the nose and throat in patients with acne with an increased carriage of S. aureus. Therefore, careful attention should be paid to the duration of tetracycline treatment in order to not increase the risk of disturbance of microbial flora.

Introduction

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Acne vulgaris is the most common disease of the skin and a chronic inflammatory disease of the pilosebaceous unit. Many factors are considered to take part in the etiology of acne; however, their effects have not been proven.1 A variety of treatment options exist for acne, including topical benzoyl peroxide, topical retinoids, topical antibiotics, oral antibiotics, hormonal therapy, and isotretinoin. Typically, oral antibiotics are indicated for moderate to severe acne cases as they show significant anti-inflammatory effects and address Propionibacterium acnes. Moreover, they may be used as an alternative treatment when other medications fail or are not tolerated by the patient. Each of these treatment options provides various benefits for the patient in the management of acne; however, their potential side effects should also be known by the healthcare provider.2 Although topical and oral antibiotics have long been in use for patients with acne, expect for those with a mild disease, it is well known that antibiotics affect diversity and composition of microflora, which has International Journal of Dermatology 2014, 53, 1404–1408

important physiological roles. Among oral antibiotics, tetracycline is considered the safest and the least expensive. The most frequently reported side effect of oral tetracycline is gastrointestinal distress such as nausea and esophagitis and skin reactions (rash, pruritus, and photosensitivity). Furthermore, vaginal candidiasis may appear with the use of tetracycline.3 Another option for recalcitrant acne or nodular cystic acne is isotretinoin or 13-cis-retinoic acid. Although teratogenic effects are the most serious, mucocutaneous side effects are the most common.4 There are many reports suggesting that the abovementioned agents may lead to changes in cutaneous and mucosal flora during treatment. It is interesting that agents used for benign conditions may lead to resistant phenotypes.5–7 Previous studies generally mention resistance against P. acnes. Even though an increase has been reported in the colonization of Staphylococcus aureus, an increase has also been reported in the number of P. acnes and Gram-negative bacilli.7–11 Microbial colonization in the human body begins soon after birth, and an average adult possesses 10 times more ª 2014 The International Society of Dermatology

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microbial cells than human cells.12 Microbial flora varies according to skin type of the human body.13 Colonization of the skin by normal skin flora is related to various factors such as age, sex, race, skin conditions, and type of colonizing strains. For instance, colonization of one area of the skin by one strain of staphylococci interferes with colonization by another species.13 Probably, normal flora of the skin has a defense mechanism against bacterial infection.12 When the immune condition is impaired or the skin is irritated or injured, non-pathogenic organisms may start to act differently and become pathogenic.13 Normal oropharyngeal flora includes aerobic and anaerobic species such as peptostreptococcus and Streptococcus viridans. Although types of staphylococcus, particularly S. aureus, could be a part of normal oropharyngeal flora, S. aureus colonization in the facial skin is often considered to be accountable for furunculosis and folliculitis.10,11 The bacterium that has the largest reservoir in the skin is coagulase-negative staphylococcus. It is also accepted as a nosocomial pathogen, particularly associated with infections in immunocompromised patients. In this study, we aimed at evaluating the effects of long-term use of tetracycline and isotretinoin as well as of topical treatment on nasal and oropharyngeal flora of patients with acne.

Flora in patients with acne vulgaris

Clinical trial

Using standard clinical techniques, oropharyngeal and nasal samples were taken from participants with the help of a sterile swab before administration of treatment and in the third month of treatment. The specimens were inoculated in 5% sheep blood agar, mannitol salt agar, and trypticase soy agar (BD Diagnostic Systems, Sparks, MD, USA). The plates were incubated at 35–37 °C for 24–48 hours. Following incubation, macroscopic examination, BBL Crystal Identification System (Gram-positive ID Kit; Becton Dickinson and Company, Sparks, MD, USA), Gram staining and coagulase testing were performed on the plates, and the colonies and their growth rate and types were identified. Types of S. aureus that were susceptible to methicillin were determined according to the criteria of the Clinical and Laboratory Institute using the Kirby– Bauer diffusion method with cefoxitin disk (301 g). Different test results arising during the treatments were compared statistically.

Statistical analyses Pearson chi-squared test, McNemar test, logistic regression test, and Fisher test were used in this study. P < 0.05 was considered significant. Statistical analyses were performed by PASW Statistics for Windows, Version 18.0 (SPSS Inc., Chicago, IL, USA).

Results Materials and methods Swab specimens were taken from right and left nasal cavities and oropharynx of 55 patients with acne vulgaris who were admitted to the dermatology department and had no history of any infectious and/or systemic disease before administration of treatment and in the third month of treatment. Patients who did not receive a previous therapy at least for one month before the referral were included in this study. Patients with acne were classified as moderate and severe according to the global acne grading system. Then, the participants of the study were divided into four groups. Group 1 included 15 patients with acne with no treatment, group 2 included 20 patients with acne who were on systemic isotretinoin, group 3 included 20 patients with acne who were on oral tetracycline, and group 4 included 20 control subjects. The control group consisted of healthy

Of 55 patients with acne, 18 were male and 37 were female. The mean age of patients and the control group was 22.21  4.22 and 21.95  7.64, respectively, and there was no statistically significant age difference between the groups (P > 0.05). Among all the patients, 36.36% had severe, 36.36% had moderate, and 27.27% had mild acne. S. aureus was detected in the naval cavity samples of five patients (25%), normal flora was suppressed in the oropharyngeal cultures of seven patients (35%), and normal flora grew in the cultures of the other 20 patients who were on tetracycline treatment. On the other hand, normal flora grew in all nasal and oropharyngeal cultures (100%) taken from patients on isotretinoin treatment. Samples that were obtained from the control subjects (Table 1) also showed normal floral growth.

volunteers who matched the patients with respect to age and gender. A routine dose of 0.5 mg/kg per day was used in treatment with isotretinoin, and the total cumulative dose was calculated to be 120 mg/kg. The patients were informed about the study, and they signed an informed consent form before participating in the study. Global acne scores were calculated for treatment options. The patients who scored between 1 and 18 were considered mild acne cases, between 19 and 30 moderate acne, between 31 and 38 severe acne, and those scoring higher than 39 very severe acne.14 ª 2014 The International Society of Dermatology

Discussion It is crucial that healthcare professionals and dermatologists who administer and prescribe acne treatments have a comprehensive overview of the side effects of various acne treatments. The most common side effects include local irritation with topical treatments whereas systemic side effects include liver function abnormalities, changes in the skin and mucosal flora, and teratogenicity with isotretinoin and tetracycline. Tetracycline, a bacteriostatic International Journal of Dermatology 2014, 53, 1404–1408

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Flora in patients with acne vulgaris

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Table 1 Results of culture that before treatment and during the third month of treatment Culture results No. of patients

Before treatment

During the third month of treatment

Patients with acne vulgaris receiving tetracycline treatment

20

Normal flora

Patients with acne vulgaris receiving isotretinoin treatment Acne patients with no treatment Control group

20 15 20

Normal flora Normal flora Normal flora

25% (5) – S. aureus was isolated from nasal flora (one of five was MRSA) 35% (7) – oropharyngeal flora was suppressed 100% normal flora 100% normal flora –

antibiotic with a broad-spectrum efficacy, which belongs to the cyclin group, is the most commonly used agent in the management of acne.1 There are studies investigating the proliferation of resistant coagulase-negative staphylococci strains in the skin flora of patients who receive acne treatment.2,5,6,14–16 Normal flora is comprised of anaerobic species such as peptostreptococcus and aerobic bacilli such as Streptococcus viridans. These organisms are rarely pathogen. Although streptococci, staphylococci, and haemophilus species constitute a part of the oropharyngeal flora, they are usually pathogens. The Gram-negative bacilli and Candida albicans are also potential pathogens.10 A study by Levy et al.17 reported that Streptococcus pyogenes colonization and resistance in the oropharynx are associated with antibiotic therapy in patients with acne. Unlike results of the present study, no significant differences were found in the resistance patterns of S. aureus in that study. Miller et al.18 evaluated carriage of staphylococci in the skin flora of patients with acne who used antibiotics for a long time as well as their resistance patterns to seven antibiotics. They looked at the changes in skin flora of patients with acne who used erythromycin, tetracycline, clindamycin, azithromycin, trimethoprim, chloramphenicol, and fusidic acid and found resistance to all antibiotics except for aminoglycosides. Unlike the results of the present study, Fanelli et al.19 reported that use of oral antibiotics in patients with acne had the strongest negative association with S. aureus colonization. They investigated S. aureus in patients with acne who used or did not use antibiotics. After 1– 2 months of use, they found an increase in the carriage of S. aureus. In addition, they determined that many of the S. aureus strains isolated from the nasal cavity were particularly resistant to clindamycin and erythromycin (40 and 44%, respectively), and a small proportion of the isolates (

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