Scientific and technological advances in medicine are prolonging the life of individuals, allowing severely ill patients to live longer, increasing the population at risk, in other words, patients with immunosuppressant conditions, making them more vulnerable to fungal infections.1-3 This population includes people with the human immunodeficiency virus (HIV), solid organ recipients or blood cell transplant and we should also take into consideration the appearance of new more potent immunosuppressants, the use of invasive therapeutic technique in intensive care units, the wide use of broad-spectrum antibiotics and the more aggressive chemotherapy for malignancies (causing mucositis and neutropenia).4,5

The incidence and severity of such infections as well as the causative pathogenic agents could be related to many risk factors of the patient such as underlying diseases, immunosuppression state and, even, the individual’s geographical location.3,6 With the introduction of more effective prophylactic strategies and the refinement in the immunosuppression regimens, the number of infectious complications after organ transplantation has been decreasing, however, infections remain as one of the life-threatening complications.6

Candidiasis is the most common fungal infection of the oral cavity, caused by fungi of the genus Candida, particularly Candida albicans, even though other species could be involved. Usually, the oral infection by Candida species is associated to immunocompromised individuals and it is characterized as an opportunistic infection.7

Oral candidiasis is among the indicators of immunodeficiency and the last decades studies in many countries have shown a change in the epidemiology of Candida spp. infections, with an increased incidence of Candida non-albicans such as C. glabrata, C. tropicalis, C. parapsilosis and C. krusei. A concerning tendency is the significant increase of strains resistance to many antifungals of the azoles and echinocandin classes. Besides, two thirds of candidemia are seen outside intensive care units.8,9 This epidemiological change has a significant impact in the therapeutic options for the initial and definitive treatment of this condition.10-12 However, the little information available regarding opportunistic infections in patients outside intensive care units are relevant to guarantee the survival of these individuals.

In view of the panorama of the problem discussed, the objective of this study is to evaluate the presence of oral candidiasis and identify the fungi of the genus candida in liver recipients, as well as analyze the association between the presence ofCandida spp. and sociodemographic, dietary habits and environmental exposure variables.

Solid organ transplant recipients are under the risk of fungal infections, many times due to the prolonged use of immunosuppressive drugs. The knowledge of the fungal species, the early diagnosis and the adequate treatment of these infections are key to improve the survival and reduce the mortality of transplant patients.4 In this study we demonstrated a prevalence of presence of Candida spp. of 39%. Levesque et al.14 investigated 52 liver transplant patients in the hospital in France and found yeasts of the genus Candida in 81% of the individuals, C. glabrata being the most prevalent species (47%). The same study demonstrated that during the period of observation, six cases of invasive candidiasis occurred in these patients. A research conducted by Rai et al.15 demonstrated 29 positive samples for the presence of Candida, Aspergillus or Alternaria as agents of secondary infections out of a total of 45 samples collected from sick patients. Solid organ transplant recipients are susceptible to opportunistic infections, therefore the correct diagnosis and the knowledge on the epidemiology of the main infectious fungus becomes important.16

Despite the lack of sufficient evidences to prove that liver transplant recipients have a higher prevalence of Candida spp. in the oral cavity compared to immunocompetent individuals, we can call attention for the need of specialized care with the oral cavity of these patients in order to avoid complications such as systemic infections caused by opportunistic microorganisms due to the use of immunosuppressive therapy after the transplant.

Infections by Candida species correspond to the larger part of invasive mycosis in the group of transplant patients.12 In this study we observed six (12%) cases of oral candidiasis, four (66%) of the atrophic type and two (33%) of the pseudomembranous type. A similar study was performed by Rojas et al.17, in which they reported a rate of 7.5% of clinical candidiasis in liver transplant recipients. In a study conducted by Gondim et al.18, the prevalence of candidiasis ranged from 3.7% to 18.7%, with the erythematous (atrophic) type being the most frequent. Rezvani et al.19 observed oral candidiasis of the erythematous type in 8.5% of the patients studied (immunosuppressed transplant recipients) and also found a percentage of 17.1% of episodes of candidiasis, with 76% of the pseudomembranous type. In another study with kidney transplant patients, 15.8% had oral candidiasis.20

These facts demonstrate that immunosuppressed patients are more vulnerable for the development of candidiasis because, despite the occurrence of infectious episodes between many studies being variable, they are more frequent in solid organ recipients.

Even though multiple studies demonstrate C. albicans as the main species isolated from patients with invasive candidiasis, we can observe a significant increase in Candida non-albicans species, particularly C. tropicalis andC. parapsilosis, and that tendency has already been noted in any situations of candidemia.21 In this study, eight species of C. albicans and 12 of Candida non-albicans were identified. A study performed by Levesque et al.14 reported 42 cultures (81%) of Candida spp., with the prevalent species being C. glabrata (47%), what demonstrates the importance of the identification of the fungal species, since Candida non-albicans species can present with a reduced sensitivity to certain conventional antifungals. In contrast to this study, the investigation conducted by Mímica et al.22 characterized 50% of the samples as C. albicans; 20.8%, C. tropicalis; 2.4%, C. krusei and 26.9%, other species (undetermined). Crocco et al.23, identified with the CHROMagar Candida technique, C. albicans in 76% of the studied samples, C. krusei in 19%, followed by C. tropicalis in 1%. Also, in Rocha et al.24research, C. albicans was the most prevalent species (86.4%), followed by C. tropicalis (4.5%). In the study by Wingeter et al.25, 93% de C. albicans were identified in the samples. These studies highlight the importance of the identification of the fungal agent in order to indicate the adequate treatment as early as possible, avoiding the risk of invasive fungal infections.26

Oral candidiasis can be considered a problem that aggravates the health of individuals with an abnormality of the immune system due to the use of immunosuppressants.21 In this study, the presence of the disease was compared to variables subjected to possible risk factors. After statistical analysis, we found that the time of the transplant was associated to the dependent variable of presence of candidiasis. In a similar study, Couto et al.27 observed that the fungal infection in patients submitted to liver transplant is dependent on some factors that can interact favoring the appearance of the disease, such as intensity of exposure to potential pathogens, degree of immunosuppression used and post-operatory care. Sun et al.28 observed that age and frequency of daily brushing of the teeth were risk factors for colonization by Candida spp., even though there was no significant relationship with the patient’s age in this study, but the values were close to significant. Regardless of the type of transplant and immunosuppressant drugs, studies highlight attention with possible risk factors, because these require different strategies for the prevention and control of Candida spp. infection.

As limitations of this study, we can report the small sample seen at the ambulatory of the hospital in the period of the study, the inclusion of patients in different stages of immunosuppression as well as the absence of a healthy control group, which hindered a design that allowed comparing between groups. This way, it would have been possible to reach more definitive conclusions when comparing the results to those of other studies.

It is important to note the results of the study on the subject can be explained by different designs, diversity in sample sizes and indicators of evaluation, besides other factors that can also be involved.

Even though the sample size is small, the results highlight the need for a more effective control of the health of these patients, particularly those with more advanced age. Besides, there was a higher incidence of the presence of Candida spp. in patients with longer time of transplant, increasing the morbidity risk in this population.

Candida species classified as non-albicans have been emerging in all fungal infections. This scenario is concerning, since the antifungal armamentarium available is very restricted and, in some cases, ineffective in infections caused by multiresistant strains. The infection reaches this severity when the correct diagnosis is not made due to the lack of laboratory standardization for the identification of fungi.

We demonstrate in the group studied that the oral cavity of liver transplant patients is being inhabited, in most part, by Candida non-albicans, what can be an alert for a more effective control of the health of these patients, particularly in those with more advanced age.

Financial support: None.

Conflict of interest: None.