Main determinants associated with candidiasis.
Abstract
Environmental, social, and economic factors are decisive for susceptibility to infectious diseases caused by opportunistic pathogens, such as Candida. Their incidence has increased significantly in recent years, mainly due to a greater number of immunocompromised people, the social and economic environment in which they develop and the current environmental crisis, climate change, which exacerbates health inequalities. Therefore, a literature review was conducted on the main social and environmental determinants of health and virulence factors as determinants of Candida spp. infection. Several studies provide valuable insights into the main predisposing determinants of Candida colonization and infection in relation to the health status of people and the virulence factors of the aetiological pathogen itself. Although there are some studies on the prevalence of Candida in different social classes, there are still few criteria to derive or claim an objective opinion on the social conditions under which this opportunistic pathogen occurs. Therefore, an overall picture that takes into account not only the intrinsic factors of the individual (human biology, health status, etc.) but also the social determinants of health, which may be related to differences in colonization and infection by different Candida species, is still lacking.
Keywords
- candidiasis
- Candida
- predisposing factors
- socioeconomic factors
- social determinants of health
1. Introduction
Lifestyle, human biology, health care, and natural and socioeconomic environment are factors that determine a person health status and are collectively referred to as social determinants of health (SDH) [1]. Different circumstances, in which people are born and develop, are crucial for the emergence and spread of emerging diseases as a result of environmental changes [2], lifestyle, human biology, and the distribution of economic resources [1, 3, 4]. Emerging diseases caused by emerging pathogens include opportunistic fungal infections, which are a major cause of morbidity and mortality and are responsible for approximately 1.5 million deaths per year worldwide [5]. The fourth most common cause of all nosocomial fungal infections associated with increased risk factors is mainly due to
Candidiasis is a disease caused by various species of the genus
2. Candida and candidiasis, an overview
Many species of the genus
Predisposing factors for candidiasis include extreme age (childhood or old age), increased concentrations of sex hormones such as estrogen in pregnancy (increased vaginal glycogen) creating a carbon-rich environment [28], occlusion of epithelial surfaces (by dentures or occlusive dressings), immune dysfunction (secondary: E.g. HIV/AIDS, leukemia, corticosteroid therapy), chemotherapy (immunosuppressants, antibiotics), endocrine diseases (diabetes mellitus), carcinomas, damaged nail folds, and others [29]. The fourth most common cause of all nosocomial infections associated with increased risk factors is mainly due to
According to various epidemiological studies, about 90% of infections caused by
3. Superficial candidiasis
In superficial mycoses, fungi colonize the outermost keratinized layers of the skin, hair, and nails [35]. They are associated with changes in the hydration and pH of the skin, mouth, throat, and other superficial tissues [7]. Superficial candidiasis is divided into cutaneous and mucocutaneous. The former can manifest as intertrigo in folds, diaper dermatitis, paronychia, and candida onychomycosis, which can be acute or chronic. Superficial candidiasis is one of the most common clinical forms and is typically chronic and recurrent; it can also be the onset of systemic infection [29]. Mucocutaneous candidiasis includes oral candidiasis, digestive tract candidiasis (which can be superficial if invasion is limited to the mucosa and submucosa) [36], vaginitis, balanitis, bronchial, and pulmonary candidiasis. Chronic mucocutaneous candidiasis and
4. Systemic candidiasis
Over 90% of deaths from mycoses or invasive fungal infections (IFI) are due to candidiasis, aspergillosis, cryptococcosis, and pneumocystosis. Invasive candidiasis, the most widespread of these, leads to severe illness and death, especially in critically ill patients and people with weakened immune systems [15, 16]. With the increasing number of invasive medical procedures and the growing number of immunocompromised patients, an increased incidence of invasive candidiasis caused by non-albicans
Primary risk factors for IFI include neutropenia with less than 500 neutrophils/ml lasting longer than 10 days, blood-related cancers, bone marrow transplants, prolonged corticosteroid treatment of more than 4 weeks, long-term ICU stays of more than 7 days, chemotherapy, HIV infection, invasive medical procedures, and recently administered immunosuppressive drugs. Other risk factors include malnutrition, solid organ transplants, severe burns, major surgery, patients receiving parenteral nutrition, and the use of intravascular catheters [26].
Invasive candidiasis, which is often associated with hospitalization, involves blood infections (candidemia) and serious infections such as intra-abdominal abscesses, peritonitis and osteomyelitis [39], pneumonia [40], ocular candidiasis [26], endocarditis [41], candiduria [42], and fungal infection in the central nervous system [43]. Almost all organs can become secondarily infected after hematogenous dissemination of the fungus [19].
5. Virulence factors and resistance
Virulence factors allow
5.1 Resistance
Years of use of antifungal and antibacterial substances in agriculture and healthcare have altered the global microbiome, leading to an increase in fungal infections that are resistant to drugs in plants, animals, and humans [37, 52].
The sensitivity to antifungal agents can differ among various
Studies, in the USA, have reported a low incidence of fluconazole resistance in
6. Environmental determinants conducive to the development of candidiasis
6.1 Adaptability to different environmental conditions and climate change
Clinically important
There are several papers of great importance reporting the presence of
On the other hand,
Global warming and climate change have a significant impact on the pathogenicity and survival of fungi, as well as on the environmental reservoir of the pathogen. Adaptation to higher temperatures increases its ability to multiply in the human body, which has a high basal temperature. This leads to an increased potential for disease, even in species previously considered nonpathogenic. This affects the spread of fungi as the increase in heat-resistant species facilitates interaction with humans, infection and transmission through skin contact, inhalation, and/or ingestion [2, 72].
7. Contamination of the clinical environment and the hands of healthcare personnel
One of the risk factors for invasive fungal infection (IFI) in immunocompromised patients is prolonged hospitalization. IFIs with
In healthcare settings, contaminated surfaces in the environment contribute significantly to the spread of infectious diseases. Despite regular cleaning, some microorganisms can form biofilms that lead to permanent contamination. In addition to reducing susceptibility to antimicrobials and biocides, biofilms also protect microorganisms from a hostile environment, including desiccation over extended periods of time [75].
In a study by Welsh et al. [76], the ability of
Although most
A study conducted by Kordecka et al. [82] in a hospital in Poland revealed a high prevalence of
7.1 HIV/aids
Both acquired and congenital immunodeficiencies can be associated with an increased susceptibility to systemic infections [26]. Immunocompromised patients have an increased risk of candidemia and deep infections with visceral disease [33].
HIV/AIDS is the most common factor associated with oropharyngeal candidiasis in children and adolescents. It is directly related to low peripheral blood CD4+ T lymphocyte counts, below 200 cells/μL, so its presence has been used as a clinical marker for infection, prior antifungal use, and changes in the oral environment [85]. In contrast to oropharyngeal candidiasis, it has been observed that patients with HIV/AIDS who develop esophageal candidiasis have lower CD4+ T lymphocyte counts [86]. The presence of oropharyngeal or esophageal candidiasis is considered an indicator of inmunosuppression [87].
7.2 Nutritional factors
The root causes of child malnutrition include lack of access to food, lack of health care, use of unsafe water and sanitation systems, and poor care and feeding practices. These underlying problems are caused by conflict, inadequate education, poverty, gender inequality, inadequate infrastructure, and other fundamental problems [88]. Globally, malnutrition is the leading of immunodeficiency and is considered a risk factor for infant death. Malnutrition has been found to increase the risk of oral colonization with
7.3 Chronic degenerative diseases
In the last decade, the increase in the immunocompromised population has led to a high incidence of invasive
In Shiraz, Iran, Zomorodian et al. [94] conducted a study on the prevalence of oral
Clinical data on candidemia in adult cancer patients reported that
The increased susceptibility of cancer patients to
7.4 Extreme age
According to the literature, the prevalence of oral candidiasis in newborns varies between 4 and 15%, with
7.5 Hygienic conditions
Candida grows on surfaces and often colonizes dentures, leading to denture stomatitis or subplate stomatitis. The diagnosis of denture stomatitis is important. According to Ibañez et al. [105], about 50% of the people in their study population with an average age of 65 to 74 years and 70% from 75 to 84 years used removable dentures. Regarding the factors associated with the development of subplaque candidiasis, in the studies conducted in different populations, the colonization of the surface of removable dentures by
Another condition that is particularly common in young children and the elderly who live in poor hygienic conditions is intertrigo caused by
7.6 Occupational exposure
There are different types of occupational hazards that can cause various clinical manifestations, most of which are superficial and cause high morbidity in the working population. A link has been observed between working conditions and dermatological diseases. An example of this is intertrigo and onychomycosis of the hands, which is not only related to the humid environment but also to contact with highly sugary foods processed by bakers, cooks, manual strawberry pickers, fruit packers, food handlers, or food shippers, in which case it is an occupational disease [20]. Leal et al. [107] investigated superficial mycoses in 21 workers of a metal smelting company, 81% of whom were infected [17] with some type of dermatomycosis. Five cases belonged to intertriginous candidiasis caused by
Silias et al. [108] carried out a study on 109 female workers (seamstresses) in a lingerie factory in Puebla, Mexico, 56 of whom had athlete’s foot. The laboratory data showed that
8. Epidemiology
The epidemiology of candidemia and the distribution of
The rapid emergence and spread resistant
Table 1 shows a summary of the main determinants of
Determinants | Main effects | References |
---|---|---|
Virulence factors | Surface molecules Biofilm Secretion of hydrolytic enzymes and toxins Dimorphism Metabolic adaptability Tigmotropism | [35, 44, 45, 46, 47, 48, 49, 50, 116] |
Antifungal resistance | Intrinsic and acquired resistance Indiscriminate use of antifungals (Varies according to each | [30, 53, 54, 55, 56, 57, 58] |
Adaptation to different environmental conditions | Beach sand, wetlands, soils (agricultural, forestry, contaminated with oil and mud), fresh water, seawater, rivers, springs, decomposing plants and vegetables, domestic and wild animals, insects | [59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71] |
Adaptation to climate change / global warming | Acclimatization to higher temperatures enhances human interaction | [2, 60, 61, 72] |
Contamination of different environments | Clinical environment (hospitalization) | [75, 76, 77, 78] |
Healthcare personnel’s hands | [79, 80, 81, 82] | |
HIV/AIDS | Oropharyngeal Candidiasis | [57, 85, 87, 117] |
Esophageal candidiasis | [86] | |
Candidemia | [26, 33] | |
Nutrition | Malnutrition | [10, 90, 91, 92] |
Iron deficiency anemia | [89] | |
Chronic degenerative diseases | DM1 | [94] |
DM2 | [94, 95] | |
Hematologic and solid neoplasms | [97, 98] | |
Age extremes | Newborns (immature immune system) | [90, 100, 102] |
Older adults (immune system weakened by aging) | [57, 103, 104, 105] | |
Hygiene | Lack of hygiene (stomatitis and intertrigo) | [105, 118] |
Occupational exposure | Superficial candidiasis (Intertrigo, onychomycosis) | [20, 107, 108] |
9. Social determinants of health in the context Candid a infection
9.1 Social determinants of health (SDH)
The World Health Organization (WHO) defines health as a state of complete physical, mental, and social well-being and not merely the absence of disease. This definition makes it possible to consider different perspectives such as the social aspects of health as social determinants of health [119].
SDH are the social, economic, and environmental conditions that influence an individual’s state of health. According to the World Health Organization (WHO), SDH such as education, housing, nutrition, work environment, access to services, unemployment, and health care are essential for equitable health. In recent years, it has also become widely accepted that the socioeconomic conditions in which people live strongly influence their chances of good health. Health and illness follow a social gradient: The lower a person’s socioeconomic position, the lower their chances of good health [120].
Poor environmental, social, and economic conditions have a negative impact on health, increase susceptibility to infectious diseases caused by emerging pathogens; these factors contribute to health inequalities that can span multiple generations. Technological advances, increasing unplanned urbanization, and climate change are new and emerging trends that may exacerbate existing inequalities and further increase inequalities in health opportunities and outcomes [121].
9.2 State of the art in DSS associated with candidiasis
One of the populations that are particularly vulnerable to opportunistic infections is those living in poverty, who suffer from precarious health conditions and have limited or no access to health facilities [122]. For example, dermatophytosis is more common in people living in crowded or promiscuous conditions such as in barracks, prisons, or nursing homes, where confined spaces favor contact with infectious material. Subcutaneous mycoses, such as mycetoma, sporotrichosis, and chromoblastomycosis, are common in underdeveloped countries, due to the fact that agricultural activities are performed manually, while in highly developed countries, they do not occur and the cases observed are imported [123]. Therefore, below are several some articles describing some social factors that favor the development of
Of the publications found describing sociodemographic characteristics or socioeconomic factors of patients colonized or infected with
Clinical manifestation | Year | Geographic region | Characteristics of the population | Related species | Prevalence (%) | DSS | References |
---|---|---|---|---|---|---|---|
Vulvovaginal Candidiasis (CVV) | 1984 | 600 obstetrics-gynecology outpatients | 43.5% (261) | Pregnancy, malnutrition, anemia, *medium socioeconomic status | [124] | ||
1995 | Pavia, Italia | 2374 gynecological patients from a vaginitis cliniC | 33.1% (786) | *Women older than 38 years, lower educational and socioeconomic levels in patients with | [125] | ||
2005 | Paraguay | 196 pediatric gynecological patients | — | *Lower-middle socioeconomic level, primary and secondary parental education | [126] | ||
2004 | Accra, Ghana | 200 patients undergoing manual vacuum aspiration | 17.2% [34] | Housing in marginal urban neighborhood | [127] | ||
2006 | Goa, India | 2432 gynecological patients | 8.5% (206) | Younger age, not being of Muslim origin, fewer children in the household, not having tap water in the house | [128] | ||
2018 | Odisha, India | 558 non-pregnant gynecological patients of reproductive age | 34% (190) | Lack of hygiene, lower educational level | [129] | ||
2014 | China | 1341 gynecological patients | 51.37% (689) | Low educational level, older age, marriage, vaginal douching | [130] | ||
2022 | 19 countries worldwide | Pregnant patients | 17–90% | Age, gestational age, parity, low educational, and socioeconomic levels | [131] | ||
2020 | Latin America | Gynecological patients of reproductive age | 20–50% | Early sexual life, socioeconomic inequality, use of contraceptive methods, multiple partners, unprotected sexual activity | [132] | ||
2012 | Detroit, MI, U.S.A. | 25 patients referred to a Vaginitis Clinic | 100% | *Married and insured white women with more than 12 years of formal education, average or above average socioeconomic level. | [133] | ||
2013 | Juiz de Fora, Brazil | 69 gynecological patients with CVV | 100% | *White women, higher education, and married. | [134] | ||
1995 | Taipei, Taiwán | 17,047 gynecological patients | 3.4% (580) | College education or higher, age in adolescence. | [135] | ||
Colonization and/or oral candidiasis | 2014 | Bolivia | 75 elderly patients | 61.3% [46] | Physiological changes, low defenses, poor hygiene, malnutrition, low income, low education. | [136] | |
2012 | México | 60 children with HIV/AIDS 60 malnourished children 57 Tarahumara children | 57.1% [36] 38.2% [27] 17.5% [11] | Immunosuppression Immunosuppression, * underlying causes — | [122] | ||
2011 | São Paulo, Brasil | 117 pediatric AIDS patients | 62% [86] | Low socioeconomic level | [137] | ||
2022 | U.S.A. | 101 infants | 48% [48] | Presence of | [138] | ||
2001 | Piracicab, SP, Brasil | 239 children | 47.3% [113] | — | [139] | ||
2019 | U.S.A. | 48 pregnant patients | 100% | Socioeconomic disadvantage, hypertension, number of decayed teeth, level of | [140] | ||
2012 | U.S.A. | 249,092 patients diagnosed with oral candidiasis | 100% | Residence in geographic areas of low socioeconomic strata, comorbid condition | [141] | ||
Nail, cutaneous and mucosal candidiasis | 2006 | México | 3749 patients from rural communities | 0.58% [22] | Marginalization | [142] | |
2006 | Manaos, Brasil | 394 with clinical suspicion of superficial mycosis | 18.3% [72] | Middle social class | [143] | ||
Candidemia | 2020 | Grecia | 522,197 hospitalized patients | 0.082% (429) | Economic crisis (limited resources for medical care), solid organ malignancies | [74] | |
2016 | U.S.A. | 225 patients with home parenteral nutrition | 6.22% [14] | Anticoagulant therapy, ulcers or open wounds, public health insurance (low socioeconomic status) | [144] |
Regarding vulvovaginal candidiasis, only 12 out of 20 studies showed any kind of positive association between socioeconomic factors and clinical manifestations. In addition, Table 1 lists these factors or determinants observed in the different populations studied. López Martínez et al. [124] conducted a study of 600 obstetric-gynecology patients to investigate opportunistic factors in vaginal candidiasis. In relation to the total population and the number of patients with a positive test for
In another study conducted in Paraguay by Laspina et al. [126] between 1995 and 1996 in 196 girls with a clinical diagnosis of vulvovaginitis, it was that the prevalence of this infection caused by
In a population-based study of women in Goa, India, Patel et al. [128] investigated the burden and determinants of reproductive tract infections in 2432 patients. The results showed a population-wide prevalence of
In 2013, Na et al. [130] conducted a study in two tropical regions of China (Hainan and Sanya) in which they investigated the risk factors associated with genital tract infection caused by
In 2022, Duran Cañarte et al. [132] investigated the most common risk factors for vaginal infections in women of childbearing age in Latin America. The results showed that the main pathogens associated with vaginal infections in women aged 15 to 40 years were
Tavares Rodrigues et al. [134] conducted a study to investigate the epidemiologic profile of patients with vulvovaginal candidiasis (VVC) in Juiz de Fora, Brazil. Of the patients studied, aged 15 to 52 years, 79.7% were white women, 58% had higher education, 56.5% were married, and 97.1% were sexually active. The study showed that the most prevalent species were
Wang et al. [135] investigated the epidemiological differences between candidiasis and trichomonads in cytological smears from 17,047 patients attending health centers and clinics in Taipei, Taiwan. The overall prevalence of
Regarding socioeconomic factors in oral
Domaneschi et al. [137] investigated the prevalence of factors associated with oral colonization by
In 2022, Alkhars et al. [138] examined
In a study conducted in the USA by Xiao et al. [140] on oral health and
In relation to the different dermatophytoses caused either by
De Oliveira et al. [143] examined 394 patients with clinically suspected superficial mycosis, 256 of whom were positive. They concluded that onychomycosis and pityriasis versicolor are the most common mycoses in the Amazon region and that
Siopi et al. [74] reported on a 10-year (2009–2018) retrospective surveillance study in a tertiary hospital in Greece that collected information on the epidemiology of candidemia, especially during severe socioeconomic events (financial crisis). The number of hospitalized patients was 522,197, among whom a total of 429 candidemia attacks were recorded.
Durkin et al. [144] conducted a descriptive observational study of 225 patients discharged with home parenteral nutrition from a hospital in St. Louis, Missouri, USA, between 2007 and 2009. Among the catheter-related complications, infections were identified in 68 patients, of which 14 (20%) involved
10. Conclusions
Several studies have been reported that provide valuable insights into the major predisposing determinants of
So, there is still a lack of a global overview that takes into account the social determinant of health in addition to the intrinsic factors of individuals (human biology, health status, etc.) that could be related to variations in colonization and infection by the different
Acknowledgments
Author Morales-Ramírez gratefully acknowledges financial support for his PhD studies from Natl. Council for Science, Technology and Humanities of Mexico (CONAHCYT).
Conflict of interest
The authors declare no conflict of interest.
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