Oral Candida colonization and candidiasis in patients with psoriasis

Vol. 114 No. 5 November 2012

Oral Candida colonization and candidiasis in patients with psoriasis Ahmad A. Bedair, BDS, MSc,a Azmi M. G. Darwazeh, BDS, MSc, PhD, FFDCRSI,b and Mustafa M. Al-Aboosi, PhD,c Irbid, Jordan ZARQA GOVERNATE HEALTH DIRECTORATE AND JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY

Objectives. The objective of this study was to investigate oral Candida colonization and candidosis in a group of patients with psoriasis and controls. Study Design. A total of 100 patients with psoriasis and matched controls underwent the concentrated oral rinse test for Candida isolation. Candida species were identified by the VITEK 2 Identification System. Categorical variables were evaluated using the ␹2 test. The median Candida count was compared using the Mann-Whitney U test. Results. Oral candidiasis was diagnosed in 3% of the patients with psoriasis. The Candida count and prevalence were significantly higher in the patients with psoriasis compared with controls (69% vs 44%, P ⬍ .001), but with no relationship to the severity or treatment of psoriasis. Oral Candida was significantly higher in late-onset (at age ⱖ30 years) compared with early-onset psoriasis (at age ⬍30 years). Conclusions. Patients with psoriasis have increased oral Candida colonization and candidiasis. Further studies are needed to clarify the predisposing factor(s) for oral Candida in patients with psoriasis. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;114:610-615)

Categorically, psoriasis is a chronic multisystem inflammatory disease, exhibiting predominantly skin and joint manifestations with variable prevalence ranging between 0.5% and 4.6%.1 Although psoriasis has a low attributable mortality, it can cause considerable morbidity and have a profound impact on the quality of patient’s life.2 Psoriasis has been classified clinically into several subtypes (phenotypes), such as plaque type, inverse, erythrodermic, pustular, guttate, psoriatic onychodystrophy, and psoriatic arthritis. The plaque type, also known as psoriasis vulgaris, is the most common form of the disease presenting in up to 90% of cases.1 The etiology of psoriasis is not precisely clear, and genetic factors,3 exogenous and endogenous environmental factors,4 and immunologic factors5 have been incriminated. There is no cure so far for this disease; however, the treatment ranges from topical therapies for mild disease, to phototherapy or systemic therapy for more This study was supported by a grant from the Deanship of the Scientific Research in Jordan University of Science and Technology (Grant no. 10/2011). a Zarqa Governate Health Directorate, Ministry of Health, Jordan. b Professor, Department of Oral Medicine and Surgery, Faculty of Dentistry, Jordan University of Science & Technology, Irbid, Jordan. c Associate Professor, Department of Internal Medicine and Dermatology, Faculty of Medicine, Jordan University of Science & Technology, Irbid, Jordan. Received for publication Jan 31, 2012; returned for revision May 5, 2012; accepted for publication May 12, 2012. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter http://dx.doi.org/10.1016/j.oooo.2012.05.011

610

widespread disease.3 This includes intense immunosuppressing agents such as methotrexate and cyclosporine.5 Several microbiological studies have shown that Candida species were isolated more frequently from stool,6 nails,7 and skin8 of patients with psoriasis than from healthy subjects. Reviewing the literature revealed that studies addressing oral Candida colonization and candidiasis in patients with psoriasis are limited and ended with conflicting results.8-10 For instance, the prevalence of oral Candida species isolation in patients with psoriasis has been reported to range widely between 23% and 78%.8-10 In addition, whether the prevalence of oral Candida carriage is higher in patients with psoriasis,10 or not,8 has not so far been clearly determined. A number of environmental factors have long been recognized to play an important role in the aggravation or exacerbation of psoriasis, including skin trauma (Koebner phenomenon), infections, stress, and humidity.4,11,12 Medications, such as calcium channel blockers,13 ␤-blockers,14 growth factors,13 antimalarials,14 indomethacin,15 and lithium salts14 also have been linked to the onset or exacerbation of psoriasis. Various microorganisms colonizing the skin or the gastrointestinal tract, including bacteria (Streptococcus pyogenes, Staphylococcus aureus), viruses (papillomavirus, retroviruses), and fungi (Malassezia, C. albicans) have been reported to trigger or exacerbate psoriasis.14 On the other hand, the question of the ability of oral Candida to trigger or exacerbate skin psoriasis has not yet been answered.10 In view of these controversial and incon-

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clusive results, this prospective study was designed to assess the qualitative and quantitative oral Candida colonization and infection in patients with psoriasis in comparison with healthy controls closely matched for age and gender. In addition, the study was designed to explore any relationship between the prevalence of oral Candida colonization or count with the clinical subtype of psoriasis, duration, onset, severity of the disease, smoking habit and type of treatment received.

MATERIAL AND METHODS The study group consisted of 100 adult patients diagnosed with psoriasis by their dermatologist. These patients were recruited consecutively from patients attending the dermatology clinics at King Abdullah University Hospital (KAUH) and Princess Basmah Hospital (PBH) in the city of Irbid located north of Jordan. Subjects who had history of antibacterial or antifungal antibiotic therapy or regular antiseptic mouth wash use over the previous 2 months or those who were wearing removable dental prosthesis or were pregnant, anemic, or diabetic were not included in the study. One hundred control subjects closely matched for age and gender were recruited from the working staff and the companions, who were not genetically related family members, of patients attending the dermatology clinic at KAUH and PBH. The control subjects fulfilled the same selection criteria as for the study group except the history of psoriasis. A subject was classified as a “smoker” when he or she reported smoking at least 1 cigarette daily over the past year. The “nonsmoker” was defined as either never having smoked, or who had quit smoking for at least 1 year before the study.16 Oral examination of the subjects was performed while seated on a chair using artificial light and sterile mirrors. All examinations and sampling were performed by one of the authors (A.A.B.). Swab and smear tests were performed on lesions suggestive for oral candidiasis, such as white pseudomembranous lesions that could be scraped off leaving an erythematous base (pseudomembranous candidiasis) and erythematous lesions associated with burning sensation (erythematous candidiasis), lip angle erythema, or cracks (angular cheilitis) or a defined white lesion that could be scraped off (candidal leukoplakia). The concentrated oral rinse technique described by Samaranayake et al.17 was used to isolate Candida species from the oral cavity. Briefly, each subject was supplied with 10 mL of 0.9% sterile normal saline in a universal container, and was asked to rinse the mouth thoroughly with the saline for a full minute, then to return the saline into the container. The rinse samples were kept in an ice box and transported

ORIGINAL ARTICLE Bedair et al. 611

immediately to the microbiology laboratory at KAUH for processing. The mouth rinse was centrifuged at 1700g for 15 minutes. The supernatant was discarded and the deposit was reconstituted in 1 mL 0.9% sterile normal saline and agitated on a vortex mixer (Assistent, Karl Hecht GmbH & Co., Germany) for 1 minute. Subsequently, 0.1 mL of the reconstituted suspension was inoculated onto plates of Sabouraud’s dextrose agar (Oxoid Ltd., Basingstoke, England). The swabs obtained from lesions clinically suspected to be oral candidiasis were streaked on similar plates. All culture plates were incubated aerobically at 37°C for 48 hours. Candida colonies were identified based on the colony color, texture, and morphology, and determination of the purity of the culture was then performed microscopically by the wet mount technique at ⫻100 objective. The number of colonies on the rinse plate was counted and multiplied by 10 to work out the number of colony-forming units per 1 mL of the rinse (CFU/mL). Any plate that contained more than one type of colony morphology was subcultured separately. Candida albicans and other species were identified using the germtube test18 and the VITEK 2 Identification System using the new colorimetric yeast cards19 (bioMérieux Inc, Durham NC). All the identification results of the Candida isolates were denoted by the VITEK 2 system as “excellent,” “very good,” “good,” or “acceptable.” No single result was described as “low discrimination,” which required supplemental tests for further identification as described in the manufacturer’s instructions.20 Smears were Gram-stained and examined microscopically under a ⫻40 objective. On the basis of Candida isolation and signs of oral candidiasis, the subjects were classified into Candida-free, asymptomatic Candida carriers, and candidiasis group. Oral candidiasis was finally diagnosed when the subject exhibited the clinical signs and symptoms of oral candidiasis in addition to the positive isolation of Candida species from the rinse and swab culture samples, and Candida blastospores or hyphae were detected in the stained smear. The subjects with oral candidiasis were referred for treatment. The severity of psoriasis was assessed by the Psoriasis Area and Severity Index (PASI) score, which was calculated by the treating dermatologist. According to the PASI score, the severity of psoriasis was categorized as “mild” when the total score calculated was less than 10, “moderate” when the total score was within the range of 10 to 20, and “severe” when the total score was more than 20.21 The study protocol was reviewed and approved by the Institutional Review Board (IRB) at KAUH in compliance with the Helsinki Declaration, and all sub-

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jects signed a detailed consent form that was also approved by the IRB. Data were analyzed using the Statistical Package for the Social Sciences (SPSS) version 17.0 (SPSS Inc., Chicago, IL). Categorical variables were evaluated using the ␹2 test. Because the numbers of CFU/mL obtained from patients with psoriasis and control subjects were not normally distributed, a Man-Whitney U test was used to compare the quantitative candidal isolation from each group. In all tests, a P value less than .05 was considered significant.

RESULTS The study and control groups each consisted of 100 subjects with a mean age of 32.9 ⫾ 14.8 years. The 2 groups were closely matched for gender and age. Each group consisted of 54 males (54%) and 46 females (46%). The mean duration of psoriasis was 10 ⫾ 8.5 years. At the time of the study, 21 (21%) patients were not receiving any treatment for psoriasis, 65 (65%) patients were on topical therapy, 6 (6%) patients were on systemic therapy, 2 (2%) patients were on phototherapy, 4 (4%) were on a combination of topical and systemic therapy, and 2 (2%) patients were on a combination of topical and phototherapy. In topically treated patients, 56 (86.1%) of 65 were medicated with topical betamethasone or calcineurin-inhibitor (tacrolimus). A total of 32 (32%) psoriatic patients were either not receiving any treatment or were on topical treatment that did not contain cortisone or immunosuppressant (i.e., emollients) or were on UVB therapy alone. This type of therapy was assumed not to predispose the patients for candidal colonization or infection. The remaining 68 (68%) patients were either on topical cortisone, methotrexate, cyclosporine, tacrolimus, and/or biological agents. This type of therapy was assumed to predispose for oral Candida colonization and infection. Three psoriatic patients (3%) showed clinical and microbiologic evidence of oral candidiasis (2 cases of erythematous candidiasis and 1 case of median rhomboid glossitis) compared with none of the control subjects. Candida albicans was isolated from rinse and culture swabs, and candidal hyphae and/or blastospores were detected on the stained smears. These 3 patients were under treatment with topical betamethasone (Daivobet), of the plaque-type psoriasis, and were nonsmokers. Candida species were isolated from the oral cavity of 69 (69%) patients with psoriasis and 44 (44%) of the control subjects with a significant difference between the 2 groups (P ⬍ .001). The median Candida count was significantly higher (P ⬍ .001) among patients with psoriasis (380 CFU/mL) compared with control subjects (150 CFU/mL). C. albicans was the most

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Table I. Candida species isolated from patients with psoriasis and control group Candida species Candida Candida Candida Candida Candida Candida Candida Candida Candida Candida Candida Candida

albicans dubliniensis kefyr glabrata famata lipolytica tropicalis krusei pelliculosa spherica zeylanoides parapsilosis

Psoriatic patients (n ⫽ 69)

Control group (n ⫽ 44)

38* (53.6%) 18 (26.1%) 3 (4.3%) 2 (2.9%) 2 (2.9%) 2 (2.9%) 1 (1.5%) 1 (1.5%) 1 (1.5%) 1 (1.5%) 1 (1.5%) 0 (0%)

22 (50%) 16 (36.4%) 2 (4.5%) 0 (0%) 0 (0%) 0 (0%) 1 (2.3%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 3 (6.8%)

*One psoriatic patient was colonized with both C. albicans and C. dubliniensis simultaneously.

commonly isolated species. Candida species were found to be more diverse in patients with psoriasis than in the control group, with 11 different Candida species in the former group compared with 5 Candida species in the latter group (Table I). The prevalence of oral candidal carriage in psoriatic patients who were smokers (25/33 [75.8%]) was slightly higher than that of the nonsmokers (44/67 [65.7%]; P ⫽ .30). Similarly, the median candidal count was insignificantly different between smokers and nonsmokers (CFU/mL ⫽ 150 versus 100 respectively; P ⫽ .33). In the control group, the prevalence of oral candidal carriage was insignificantly different between smokers (6/22 [27.3%]) and nonsmokers (38/78 [48.7%]; P ⫽ .07). The median candidal count was also insignificantly different between smokers (CFU ⫽ 85) and nonsmokers (CFU ⫽ 100; P ⫽ .09). Because of the small numbers of Candida carriers among some psoriasis clinical subtypes (⬍5 subjects), the qualitative and quantitative oral Candida colonization was compared between patients with plaque-type and nonplaque-type psoriasis. The statistical analysis showed an insignificant difference in either qualitative or quantitative oral Candida colonization between patients with plaque-type and nonplaque-type psoriasis (Table II). As shown in Table II, the quantitative and qualitative oral Candida colonization was significantly higher in patients with psoriasis with late-onset disease (at age ⱖ30 years) compared with those with earlyonset disease (at age ⬍30 years). Neither the duration of the disease nor the treatment modality affected the oral candidal colonization in patients with psoriasis (Table II). The PASI score was calculated for 89 (89%) of patients with psoriasis, whereas the remaining 11 (11%) patients refused to show the lesions involving the covered portions of their bodies. Of these 89 pa-

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ORIGINAL ARTICLE Bedair et al. 613

Table II. Oral Candida colonization in different subgroups of psoriatic patients Groups Psoriasis subtype Plaque (n ⫽ 85) Nonplaque (n ⫽ 15) Psoriasis duration ⬍10 years (n ⫽ 51) ⱖ10 years (n ⫽ 49) Onset of psoriasis ⬍30 years (n ⫽ 72) ⱖ30 years (n ⫽ 28) Treatment modality Not treated (n ⫽ 21) Treated (n ⫽ 79) Psoriasis severity* Mild (n ⫽ 61) Moderate (n ⫽ 18) Severe (n ⫽ 10)

Oral Candida isolation n (%)

P

Median [range] Candida count (CFU/mL)

P

59 (69.4) 10 (66.7)

0.83

140 [20-5000] 160 [30-3500]

0.78

35 (68.6) 34 (69.4)

0.93

100 [20-5000] 270 [10-5500]

0.1

45 (62.5) 24 (85.7)

0.02

85 [10-5000] 890 [10-5000]

⬍0.000

17 (80.9) 52 (65.9)

0.18

210 [20-5500] 130 [30-5000]

0.61

43 (70.5)† 13 (72.2)† 6 (60.0)†

0.71

140 [30-5000] 140 [40-3600] 235 [30-5200]

0.77

CFU, colony-forming unit. *PASI score was performed for 89 patients only. † One-way analysis of variance.

tients, Candida species were isolated from the oral cavity of 62 (69.7%) patients, whereas 27 (30.3%) patients were Candida-free. The mean PASI score of psoriatic patients who were colonized with Candida species (8.8 ⫾ 9.8) was not significantly different from those who were Candida-free (9.4 ⫾ 8.1; P ⫽ .73). In addition, the severity of the disease had no relationship to either the prevalence or the median count of oral candidal colonization in patients with psoriasis (Table II). In the multivariate analysis, the only factor significantly associated with oral Candida colonization was the psoriasis-onset status. After adjustment for the effects of other variables, including gender, age, smoking status, the subtype of psoriasis, treatment of psoriasis (treated versus not treated, predisposing versus nonpredisposing treatment), and the duration and the severity of the disease, psoriasis with late onset (ⱖ30 years of age) was significantly associated with increased odds of colonization. Patients with late-onset psoriasis were 8 times more likely to have oral Candida colonization (P ⫽ .048) compared with patients with early-onset psoriasis (⬍30 years of age). Candida species were isolated with comparable prevalence from psoriatic subjects who were either not receiving treatment for their psoriasis or on treatment not known to predispose to oral candidiasis (22/32 [68.8%]) as those who were receiving treatment known to predispose to oral candidiasis (47/68 [69.1%]; P ⫽ .97). Similarly, there was no significant difference in the median candidal counts between these 2 groups of psoriatic subjects (CFU/mL ⫽ 120 versus 145 respectively; P ⫽ .71). Geographic tongue and fissured tongue were detected in 17 (17%) and 35 (35%) of the psoriatic pa-

tients, respectively. Geographic tongue was diagnosed in 10 (14.5%) of 69 and in 7 (22.6%) of 31 of patients with psoriasis who were colonized with Candida species and in those who were Candida-free respectively (P ⫽ .32). In addition, there was no significant difference in the prevalence of fissured tongue between patients with psoriasis colonized with Candida species (25/69 [36.2%]) and Candida-free patients (10/31 [32.3%]; P ⫽ .7).

DISCUSSION The literature on oral Candida colonization and infection in patients with psoriasis is limited and ambiguous. Henseler22 reviewed the medical records of 44,695 dermatologic patients and concluded that psoriatic patients had 1.3 to 1.6 relative risk of developing mucocutaneous candidiasis compared to healthy persons. Skinner et al.23 reported 14 psoriatic patients in whom the disease was associated with oropharyngeal Candida. Studies surveying oral lesions in psoriatic patients have reported angular cheilitis24 and erythematous and pseudomembranous candidiasis25 in 11.0% and 8.7% of the patients respectively. Our finding of oral candidiasis in 3% of psoriatic patients but in none of the closely matched healthy control subjects suggests that psoriatic patients may be slightly predisposed for oral candidosis.25 In view of lack of relationship of oral candidiasis to the immunosuppressive therapy, more studies are needed to confirm this finding and to elucidate an explanation. Our finding of significantly higher prevalence and count of oral Candida in patients with psoriasis supports the results of previous studies.8,10 Relevantly, a higher level of Candida colonization was reported in other body parts in patients with psoriasis,

ORAL MEDICINE 614 Bedair et al.

such as the intertriginous area,26 gastrointestinal tract,3 and nails.27 Using the concentrated oral rinse technique for candidal isolation, our finding of 69% oral Candida carriage rate is consistent with the 78% carriage rate reported by Waldman et al.10 who cultured saliva. However, as low as 47.7%28 and 32.0%9 oral Candida carriage rates were reported using a tongue swab culture technique. This latter technique is generally known for its relatively lower sensitivity in candidal isolation. Putting these data together is consolidating the notion that psoriasis can be one of the systemic diseases that predispose to oral Candida carriage and infection. Nevertheless, if this observation is confirmed by further studies, it still waits explanation. In this regard, immunologic studies reported reduction in the number of the circulating natural killer cells in psoriatic patients compared with controls,29 whereas others observed no difference.30 Methotrexate and cyclosporine, the intense immunosuppressive agents, are the most widely used systemic agents in psoriasis management.3 These agents are also well known for their predisposition to oral candidal infections.31,32 Surprisingly, the oral candidal colonization in our study was not affected by the mode of the patient’s therapy. The adhesion of microorganisms to host mucosal surfaces has been long recognized as a necessary prerequisite for successful microbial colonization and subsequent infection.33 The frequently reported increased prevalence of oral candidal colonization and infection in patients with diabetes mellitus was explained partly by the higher affinity of their oral epithelial cells to yeast cells.34 Therefore, it is tempting to investigate the adhesion of C. albicans and other species to oral epithelial cells from psoriatic patients in comparison with healthy subjects. In the current study, C. albicans was the predominant oral Candida isolate constituting approximately 64% of the species isolated. Similarly, Candida species were shown to be significantly more prevalent in the intestinal tract (the other end of the alimentary tract) of the patients with psoriasis, and C. albicans was the predominant species isolated.6,35 Further Candida phenotyping studies are encouraged to clarify the precise interrelationship of oral, skin, and intestinal Candida colonization in patients with psoriasis. C. albicans accounts for approximately 50% of the oral isolates in the general population. In the past 2 decades, a higher incidence of non-albicans species has been reported, particularly in immunocompromised subjects.36 This observation was explained by the emergence of improved microbiologic diagnostic methods in addition to the wide-spread use of immunosuppressive agents,37 which also may explain partly our observation of higher incidence of non-albicans species isolation in pso-

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riatic patients. Future comparative candidal-mucosal adhesion studies, using different Candida species may shed light on this area. The provocation and exacerbation of psoriasis has been claimed to be triggered by various microorganisms.14 Some studies have not found strong evidence suggestive of a relationship between Candida isolated from the oral cavity,6,9,10 intestine,35 or skin38 and the severity of psoriasis. Indirectly, Soyuer et al.,35 using indirect hemagglutination and indirect immunofluorescence tests, did not find a correlation between the titer of anti-Candida antibodies and PASI score in 39 patients with psoriasis. In our findings, the qualitative and quantitative oral Candida colonization did not have significant relationships with psoriasis clinical subtype, age, gender of patients, and duration, which was similar to the findings of another study.9 Nevertheless, there was a significant increase in Candida isolation from relatively late-onset psoriasis (ⱖ30 years) compared with early-onset disease (⬍30 years). Based on the available data, this latter observation could not be explained. The current data showed that tobacco smoking did not affect oral Candida colonization in patients with psoriasis or the control subjects, which is consistent with the results of previous studies that concluded the lack of association between smoking and oral Candida in healthy adults.16 There is strong evidence that some atrophic tongue lesions, such as median rhomboid glossitis, are eminently associated with candidal infection39; however, geographic tongue and fissure tongue are widely accepted as noncandidal oral mucosal lesions.40 In our study, the cases diagnosed with geographic or fissured tongue in patients with psoriasis were not linked to positive isolation of Candida species. In the view of the current results, larger scale studies are warranted to clarify the precise factor(s) predisposing patients with psoriasis for increased oral candidal colonization. Oral health care providers should be aware of this predisposition and the possibility of developing oral candidiasis in patients with psoriasis. The authors thank Dr. Yousef A. Khader, Associate Professor in the Department of Public Health, Community Medicine and Family Medicine, Faculty of Medicine, Jordan University of Science and Technology for his valuable advice and help in the statistical analysis of the results. REFERENCES 1. Griffiths CE, Barker JN. Pathogenesis and clinical features of psoriasis. Lancet 2007;370:263-71. 2. Basavaraj KH, Navya MA, Rashmi R. Stress and quality of life in psoriasis: an update. Int J Dermatol 2011;50:568-72. 3. Galadari I, Sharif MO, Galadari H. Psoriasis: a fresh look. Clin Dermatol 2005;23:491-502.

OOOO Volume 114, Number 5 4. Chandran V, Raychaudhuri SP. Geoepidemiology and environmental factors of psoriasis and psoriatic arthritis. J Autoimmun 2010;34:314-21. 5. Krueger G, Ellis CN. Psoriasis—recent advances in understanding its pathogenesis and treatment. J Am Acad Dermatol 2005;53:S94-100. 6. Buslau M, Menzel I, Holzmann H. Fungal flora of human faeces in psoriasis and atopic dermatitis. Mycoses 1990;33:90-4. 7. Szepietowski JC, Salomon J. Do fungi play a role in psoriatic nails? Mycoses 2007;50:437-42. 8. Henseler T, Tausch I. [Mycoses in patients with psoriasis or atopic dermatitis.] Mycoses 1997;40:22-8. German. 9. Leibovici V, Alkalay R, Hershko K, Ingber A, Westerman M, Leviatan-strauss N, Hochberg M. Prevalence of Candida on the tongue and intertriginous areas of psoriatic and atopic dermatitis patients. Mycoses 2008;51:63-6. 10. Waldman A, Gilhar A, Duek L, Berdicevsky I. Incidence of Candida in psoriasis—a study on the fungal flora of psoriatic patients. Mycoses 2001;44:77-81. 11. Menter A, Gottlieb A, Feldman SR, van Voorhees AS, Leonardi CL, Gordon KB, et al. Guidelines of care for the management of psoriasis and psoriatic arthritis: section 1. Overview of psoriasis and guidelines of care for the treatment of psoriasis with biologics. J Am Acad Dermatol 2008;58:826-50. 12. Benoit S, Hamm H. Childhood psoriasis. Clin Dermatol 2007;25:555-62. 13. Naldi L, Gambini D. The clinical spectrum of psoriasis. Clin Dermatol 2007;25:510-18. 14. Fry L, Baker BS. Triggering psoriasis: the role of infections and medications. Clin Dermatol 2007;25:606-15. 15. Kawada A, Tezuka T, Nakamizo Y, Kimura H, Nakagawa H, Ohkido M, et al. A survey of psoriasis patients in Japan from 1982 to 2001. J Dermatol Sci 2003;31:59-64. 16. Darwazeh AM, Al-Dwairi ZN, Al-Zwairi AA. The relationship between tobacco smoking and oral colonization with Candida species. J Contemp Dent Pract 2010;11:17-24. 17. Samaranayake LP, MacFarlane TW, Lamey PJ, Ferguson MM. A comparison of oral rinse and imprint sampling techniques for the detection of yeast, coliform and Staphylococcus aureus carriage in the oral cavity. J Oral Pathol 1986;15:386-8. 18. MacKenzie DW. Serum tube identification of Candida albicans. J Clin Pathol 1962;15:563-5. 19. Graf B, Adam T, Zill E, Göbel UB. Evaluation of the VITEK 2 system for rapid identification of yeasts and yeast-like organisms. J Clin Microbiol 2000;38:1782-5. 20. Loïez C, Wallet F, Sendid B, Courcol RJ. Evaluation of VITEK 2 colorimetric cards versus fluorimetric cards for identification of yeasts. Diagn Microbiol Infect Dis 2006;56:455-7. 21. Vedhara K, Morris RM, Booth R, Horgan M, Lawrence M, Birchall N. Changes in mood predict disease activity and quality of life in patients with psoriasis following emotional disclosure. J Psychosom Res 2007;62:611-9. 22. Henseler T. [Mucocutaneous candidiasis in patients with skin diseases.] Mycoses 1995;38:7-13. German. 23. Skinner RB, Rosenberg EW, Noah PW. Psoriasis of the palms and soles is frequently associated with oro-pharyngeal Candida albicans. Acta Derm Venereol 1994;186:149-50. 24. Buchner A, Begleiter A. Oral lesions in psoriatic patients. Oral Surg Oral Med Oral Pathol 1976;41:327-32.

ORIGINAL ARTICLE Bedair et al. 615 25. Perez FH, Aveldanez AJ, Ruvalcaba MU, Barcelot MD, Camacho MI, Memije MV, et al. Prevalence of oral lesions in patients with psoriasis. Med Oral Patol Oral Cir Bucal 2008;13:e703-8. 26. Rebora A. Candida and psoriasis. Letter to the editor. Acta Derm Venereol 2003;48:175. 27. Leibovici V, Hershko K, Ingber A, Westerman M, LeviatanStrauss N, Hochberg M. Increased prevalence of onychomycosis among psoriatic patients in Israel. Acta Derm Venereol 2008;88:31-3. 28. Senff H, Bothe C, Busacker J, Reinel D. Studies on the yeast flora in patients suffering from psoriasis capillitii or seborrhoic dermatitis of the scalp. Mycoses 1990;33:29-32. 29. Koreck A, Surányi A, Szöny BJ, Farkas A, Bata-Csörgö Z, Kemény L, Dobozy A. CD3⫹CD56⫹ NK T cells are significantly decreased in the peripheral blood of patients with psoriasis. Clin Exp Immunol 2002;127:176-82. 30. Cameron AL, Kirby B, Fei W, Griffiths CE. Natural killer and natural killer-T cells in psoriasis. Arch Dermatol Res 2002; 294:363-9. 31. Al-Mohaya MA, Darwazeh AM, Bin-Salih S, Al-Khudair W. Oral lesions in Saudi renal transplant patients. Saudi J Kidney Dis Transpl 2009;20:20-9. 32. Feld R. The role of surveillance cultures in patients likely to develop chemotherapy-induced mucositis. Support Care Cancer 1997;5:371-5. 33. Gibbons RJ, Houte JV. Bacterial adherence in oral microbial ecology. Annu Rev Microbiol 1975;29:19-44. 34. Darwazeh AM, MacFarlane TW, Lamey PJ. The in vitro adhesion of Candida albicans to buccal epithelial cells (BEC) from diabetic and non-diabetic individuals after in vivo and in vitro application of nystatin. J Oral Pathol Med 1997;26:233-6. 35. Soyuer U, Kilic H, Alpan O. Anti-Candida antibody levels in psoriasis vulgaris. Cent Afr J Med 1990;36:190-2. 36. Krcmery V, Barnes AJ. Non-albicans Candida spp. Causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect 2002;50:243-60. 37. Falagas ME, Roussos N, Vardakas KZ. Relative frequency of albicans and the various non-albicans Candida spp among candidemia isolates from inpatients in various parts of the world: a systematic review. Int J Infect Dis 2010;14:e954-66. 38. Miura H, Sano S, Higashiyama M, Itami S, Yoshikawa K. Candida is not involved in the development of periungual psoriatic lesion. J Dermatol Sci 1998;18:64-5. 39. Wright BA, Fenwick F. Candidiasis and atrophic tongue lesions. Oral Surg Oral Med Oral Pathol 1981;51:55-61. 40. Guggenheimer J, Moore PA, Rossie K, Myers D, Mongelluzzo MB, Block HM, et al. Insulin-dependent diabetes mellitus and oral soft tissue pathologies. I. Prevalence and characteristics of non-candidal lesions. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:563-9. Reprint requests: Professor Azmi M. G. Darwazeh Faculty of Dentistry Jordan University of Science & Technology PO Box 3030 Irbid 22110, Jordan [email protected]