FormalPara Key Summary Points

Healthcare disparities are a multifaceted issue that include socioeconomic, political, ethnic/racial, and regional factors

Publications about healthcare disparities in atopic dermatitis (AD) in Latin America (LA) and other parts of the world are scarce, and identifying and addressing healthcare disparities is critical to improving the care and quality of life (QoL) of patients with AD

To create this narrative review, a panel of pediatric allergists and dermatologists were convened by AHF and spent 3 days reviewing the literature and discussing their real-world experience to address barriers for health equity in AD and suggest steps to overcome them

Many factors impact QoL for people with atopic dermatitis, and the impact is greater for those who are less educated, earn less money, and live in poorer neighborhoods

The authors propose collaborative networks among LA countries, local living guidelines, extension programs from colleges that interact with people who have cultural or language barriers, fostering patient education programs, and using technology, specifically telemedicine, to reach patients to reduce health disparities in LA

Introduction

Atopic dermatitis (AD) is a chronic, pruritic, multifactorial, and heterogeneous inflammatory skin disease involving genetic, immunological, and environmental factors, characterized by periods of exacerbation and remission. AD occurs predominantly in childhood but can also affect adults, and the disease is not limited to patients of a specific gender or ethnicity. A family history of atopic diseases is a strong predictor of AD, indicating that genetic factors play a role in its development [1]. The multifaceted etiology of AD includes defects in the skin barrier, skin dysbiosis, and a dysregulated immune system [2]. About one-third of people with AD also have allergic manifestations like asthma, food allergies, rhinitis, and conjunctivitis [3, 4]. Besides skin lesions, AD is linked to various systemic inflammatory illnesses, sleep disturbances, neuropsychiatric disorders, and increased risk of cardiovascular disease [5, 6].

In Latin America (LA), the prevalence of AD ranges from 5% to 25%. Studies reported that 60–70% of cases develop during the first year of life, and 90% of all cases are diagnosed in the first 5 years. In 2004, the International Study of Asthma and Allergies in Childhood (ISAAC) established the prevalence of AD between 5% and 10% in children aged 6 and 7 years in LA [7]. The natural history of the disease for most patients is that AD goes into remission in adolescence and adult life. However, 10–30% of patients continue to have symptoms of the disease in adulthood, and in some patients (3–4%) the onset of AD is during adolescence or after adulthood. AD prevalence in adults is 1–3% [8,9,10,11].

Healthcare disparity is a complex issue encompassing socioeconomic, political, ethnic/racial, and regional factors. Publications about healthcare disparities in AD in LA and other parts of the world are scarce. Therefore, identifying and addressing healthcare disparities is of utmost importance to improve the care and quality of life (QoL) of patients with AD.

The issue of healthcare disparity has been gaining momentum, likely due to the COVID-19 pandemic, increasing socioeconomic inequality and ethnic/racial tensions around the world. The term “health disparity” was coined in the USA around 1990 and denoted a specific disparity: substandard health in disadvantaged racial/ethnic groups [12]. However, beyond the racial/ethnic and sociopolitical perspective, the Agency for Healthcare Research and Quality (AHRQ) defines healthcare disparities in broader terms as “differences in access to or availability of medical facilities and services, and variation in rates of disease occurrence and disabilities between population groups defined by socioeconomic characteristics such as age, ethnicity, economic resources, or gender and populations identified geographically” [13]. This definition encompasses the complexity of healthcare disparity with its implications and interconnections. This paper aims to examine the barriers to equal access to care for AD in LA and recommend realistic actions to overcome them.

Methods

The Americas Health Foundation (AHF) gathered a panel of six pediatric dermatologists and allergists from Argentina, Brazil, Colombia, Chile, Mexico, and Uruguay. They held a 3-day conference on 20–22 April 2022 to generate proposals for reducing the disparities in access to AD diagnosis and treatment in LA. AHF searched PubMed, MEDLINE, and EMBASE for AD-published allergists and dermatologists in LA. AHF supplemented this search by contacting thought leaders in the LA medical community to ensure that the list appropriately reflected the relevant areas. This manuscript’s authors include all the specialists who attended the conference.

The authors researched AD through PubMed, MEDLINE, and EMBASE. “Treatment,” “diagnosis,” “quality of life,” “patient journey” in combination with “Latin America,” “atopic dermatitis,” “inequity,” and “health disparities” were searched with dates ranging from 01/01/2016 until 2/10/2022. The articles identified were in English, Portuguese, and Spanish. Literature and research from LA were prioritized.

AHF prepared specific questions to address health inequities that restricted access to AD diagnosis and treatment in LA and allocated one to each panel member. Individual panel members submitted written responses to their questions on the basis of the literature and their knowledge. During the 3-day meeting, the panel scrutinized and modified each account through multiple debate rounds until all panelists agreed. The panel unanimously endorsed the recommendations on the basis of the facts obtained, professional opinion, and personal experience. The completed paper was sent to the panel for evaluation and approval after the conference. The authors maintain editorial control over the paper’s content. This article is based on previously conducted studies and does not contain any new studies with human participants or animals performed by any of the authors.

Results

Impact on Quality of Life (QoL) for Patients with Atopic Dermatitis

Neuropsychological and Emotional Impact

The symptoms associated with AD, pruritus being the most common, profoundly impact the QoL of patients and their caregivers, affecting sleep quality and impairing school and work productivity. Anxiety, depression, ADHD, suicidal ideation, and sleep deficit disorder are just a few neuropsychological symptoms patients with AD can experience. [14, 15].

Economic Impact

The economic impact of AD is directly related to disease severity. There are considerable disparities in LA regarding drug costs and healthcare access [16]. In Colombia, Mexico, and Peru, the expenses per patient in 2021 for topical treatment, systemic steroids, absenteeism, laboratory tests, and medical appointments ranged from US $443.00 to US $6360.50, not including biological treatments or immunosuppressants [17].

Environmental Factors

Climate and geography in LA are variable, with broad temperature and humidity ranges, and recent evidence shows that climate change may influence AD prevalence and severity [10, 18]. Air pollution, factory emissions, and water hardness have been associated with an increased frequency of AD and other allergic diseases [19, 20]. Children living near factories in Buenos Aires, Argentina, were twice as likely to have AD [21, 22].

Discussion

Ways to Improve QoL

Guidelines in Place to Aid Healthcare Professionals

Despite advances in our understanding of the pathogenesis of AD and the introduction of new treatments, managing this disease remains a challenge for both patients and doctors. To this day, AD is a disease that continues to have multiple names and many diagnostic and severity criteria. It is not surprising that AD care and treatment standards vary widely.[23,24,25] This variability has led experts worldwide to emphasize the need to harmonize AD diagnosis, outcome measures, treatments, and other topics, resulting in an upsurge of consensus meetings, reports, and clinical practice guidelines (CPGs) [26, 27]. In recent years, the quantity of CPGs has led to the generation of systematic reviews of AD CPGs to evaluate their quality, similarities, discrepancies, and applicability [26]. These reviews have shown that “not all guidelines are created equal,” and many have divergent recommendations, suffer from bias, lack applicability, and have recommendations that are not evidence based.

LA has not been an exception to increased AD research and development [17]. Several CPGs exist in the region for diagnosing and treating AD, including a multinational guideline by the Latin America Allergy, Asthma and Immunology Society (SLAAI), and national guidelines in Mexico, Colombia, Argentina, and Brazil [28,29,30,31,32,33].

Lack of consistent guideline implementation results in underestimation or overestimation of AD diagnosis. Although all guidelines recommend topical steroids as the primary symptomatic treatment for AD, researchers discovered that, particularly in managing children, primary care physicians (PCPs) and their caregivers had a fear of corticosteroids (corticophobia) negatively affecting the control of AD symptoms [34]. Researchers reported that PCPs provided heterogeneous care for AD; for example, many performed unnecessary food restrictions, impacting children’s nutrition [35].

Access to Therapeutics

Health disparities disproportionately affect patients in underserved groups, and these disparities are linked to economic, environmental, and social disadvantages. Physicians’ academic training may not always consider the characteristics of disadvantaged racial and ethnic groups. [36] More robust educational opportunities are needed to fully equip trainees with tools to recognize and develop effective strategies to reduce the burden of health disparities. The segregation of groups by race, culture, or geographic location generates limitations in access to the healthcare system, and restricted access seems to result in more severe forms of the disease [37, 38].

AD management should follow a comprehensive, stepwise approach tailored to disease severity. First-line management involves educational programs, psychosocial support, appropriate skincare, avoidance of triggers, antimicrobials, antiseptics, topical corticosteroids (TCS), and other agents such as topical calcineurin inhibitors (TCI). Second-line management includes phototherapy, especially ultraviolet (UV) A and narrowband ultraviolet B (NBUVB), and intensive topical treatment. Most AD cases are controlled by limiting exacerbating factors, maintaining proper skin care, and using topical treatments [28, 30, 33, 39,40,41,42]. However, for severe or non-respondent disease, systemic immunosuppressants, biologics, and inhibitors of Janus kinases (JAK) may be needed. As more effective, targeted treatments emerge, correct diagnosis and an appropriate assessment of severity are essential to determining the best strategies for control.

Skin Care Measures

Appropriate skin care is essential for all patients with AD [28, 30, 33, 39, 41,42,43]. Regular moisturizer use increases skin hydration [44,45,46] and may reduce the dose of antiinflammatory treatments, such as TCS, required for disease control [46, 47]. Soap substitutes, including synthetic detergents (syndets) with neutral or acidic pH and mild surfactants, minimize the damage to skin proteins and lipids induced by regular alkaline soaps [48, 49]. However, in some countries in LA, skin care products such as emollients and soap substitutes are not regularly covered by the healthcare system (Table 1a).

Table 1 Systemic treatments in Argentina, Brazil, Chile, Colombia, Mexico, and Uruguay

Topical Antiinflammatory Therapy

TCS are considered the mainstay of antiinflammatory therapy in AD, especially in managing acute flare-ups, but also in proactive, intermittent use as maintenance therapy. However, the availability of TCS may be limited in LA countries, particularly in public healthcare (Table 1a).

When TCS are not well tolerated or in locations such as the face or neck, TCI (e.g., tacrolimus and pimecrolimus) may be prescribed. TCI has proven efficacy in AD in active and proactive treatment. [50,51,52] Like TCS, the availability of TCI may be restricted in some LA countries, especially in public healthcare. (Table 1a).

Treatment for Moderate-to-Severe AD

Upscaling to phototherapy or systemic agents is indicated if the condition does not respond to topical treatment.

Phototherapy

Phototherapy is recommended as second-line or adjuvant therapy in patients with moderate-to-severe AD, especially in adults and older children.[53] The best efficacy was NBUVB (311–313 nm) and UV A-1 (340–400 nm) [54,55,56].

Phototherapy is not easily accessible in LA, and there is limited equipment availability, primarily due to high costs. This office-based therapy is only offered in some public hospitals and private centers, and it is often not convenient for those patients who live far away from a phototherapy facility (Table 1a).

Systemic Immunosuppressant Agents

Third-line treatments for moderate-to-severe AD include cyclosporine, methotrexate, azathioprine, and mycophenolate mofetil [43, 57]. When prescribing systemic immunosuppressant agents (SIS), many variables must be considered, including comorbidities and baseline laboratory results. SIS are associated with potentially severe adverse effects and require strict clinical and laboratory monitoring. Therefore, candidates for systemic therapy must be carefully selected. Sharing information about treatment efficacy and potential side effects with the patient and caregivers is also very important. Appropriate indication and follow-up for SIS require considerable time, which may limit their use. In addition, the high cost of some of these agents [57] may limit their use in some LA countries, especially in public hospitals and rural healthcare facilities (Table 1b).

Biologics and Small-Molecule Therapies

Several emerging therapies show efficacy and short-term safety that are potentially superior to traditional SIS. Systemic biologic therapy, like dupilumab and other agents, as well as small-molecule agents, such as JAK inhibitors, are appropriate in moderate and severe AD to improve disease response and QoL and limit disease progression [58, 59].

Dupilumab is available in several countries in LA, but in some of them it is not approved for AD or not approved for pediatric use. Similarly, only a few LA nations have approved JAK inhibitors, and their high expense further limits who has access to them. Also, most healthcare systems require an objective instrument to quantify disease to access high-cost medications. This is an additional limitation because most physicians in LA are not trained in applying AD scoring methods [28]. The accessibility to new and expensive therapies for AD, and their impact on the healthcare systems in LA, will have to be addressed.

Access to PCPs and Specialists if Necessary

Two objectives in the clinical management of AD are achieving clinical control and preventing complications. These objectives are achieved with adequate patient access to health networks [60, 61]. PCPs are usually trained to diagnose and treat the most prevalent diseases in their clinical practice. So, they rely on specialists, especially for severe or difficult-to-treat cases.

Access to AD specialists in LA appears to be limited [62]. Factors affecting access include lack of specialists, high patient volume, time constraints, economic barriers, lack of patient knowledge to consult about AD, or PCPs’ lack of awareness of AD. Difficulty accessing specialists becomes a barrier to controlling AD, which hurts patient treatment. A better understanding of the causes of this access issue could be the first step to proposing practical solutions.

Barriers Leading to Health Disparity and Lower QoL in People with AD.

Barriers to Specialist Access

Our extensive literature search in Spanish, Portuguese, and English yielded just eight papers on barriers to accessing the healthcare system in LA, none of which were specific to AD. Despite this, the identified papers provided insight into possible access barriers to AD specialists. Access to the healthcare system in Latin American countries is diverse and uneven [63]. In some countries, registration with the national health system is mandatory, so 100% of the population has at least a primary healthcare network to access regardless of income [64]. In other Latin American countries, registration is not required [64].

Most LA countries have a mixed (public and private) healthcare system. Depending on the country, public access to a specialist involves meeting several requirements, generating access inequality between populations [63].

In all countries in LA, access to specialists by private practice is available [63] but in some countries, the public healthcare system (PHS) allows access to PCPs and specialists only upon referral. In contrast, in others, the PHS has additional restrictions on access to specialists, for example, only in medical emergencies [16] As most countries in LA have a low or medium per capita income, patient cost is often a barrier to correct AD management[65].

Sometimes cultural, geographic, and social characteristics impede access to healthcare. Although countries such as Brazil and Colombia have a public healthcare network, its use varies according to whether the person lives in a rural or urban area [66, 67]. Access to healthcare centers in rural areas is a challenge, presumably due to centers being more distant and patients needing to take additional unpaid time off from work with added travel expenses. Some ethnic groups in closed communities seem to have less confidence in the medical treatments offered by the state, especially among the native communities that are abundant in LA and prefer to use traditional medicine [68,69,70]. In addition, language and cultural barriers exist in certain communities because the needs or the way of approaching the problem may differ from what the treating physician has in mind [71].

One of the panelists surveyed allergists and dermatologists from LA in a convenience sample taken between March and April 2022 to better understand their perception of AD management in Latin American countries. An overwhelming majority of those surveyed (98.3%) did not believe PCPs or first points of contact are sufficiently trained to diagnose AD and recognize appropriate referral situations. About one-third of those surveyed (35%) perceived that there are insufficient allergists and dermatologists to cover the demand for patients with AD in LA.

According to reports from allergy and dermatology societies in LA, the number of specialists per 100,000 inhabitants was highly variable [17], with dermatologists ranging from 1.2 in Mexico to almost 9.2 in Uruguay, while allergists ranged from 0.2 in Peru to 5.7 in Argentina. These heterogeneous results are partly due to the lack of training in medical schools in some countries.

In each country in LA, the ideal number of medical specialists depends on several factors. The barriers to access previously discussed mean that some populations cannot access specialists. On the other hand, in countries with a robust healthcare system that makes it easier to overcome these barriers, there will be more patients diagnosed who need to be managed for their AD. Therefore, a higher number of doctors are required to care for them.

Despite significant advances in understanding AD pathophysiology and new drugs and treatments, AD management remains challenging for patients and doctors. Patients with AD and their caregivers are often confused and frustrated by the information they receive from healthcare providers (HCPs) and online sources.

Online surveys in Argentina and Brazil showed that 40% and 80% of patients with AD and their caregivers expressed dissatisfaction with their treatment. Patients complained that doctors do not know how to manage the disease and fail to provide adequate information and emotional support [72].

Socioeconomic Parameters

Income inequality and poverty remain major challenges in LA. The correlation between the prevalence of AD symptoms and socioeconomic status should be interpreted with caution since local data from each center may differ substantially from national data. However, to our knowledge, no studies have addressed this issue in LA.

Nutrition

LA is one of the world regions with the most significant disparities in access to a balanced diet, and deficiencies in specific nutrients could contribute to the pathophysiology of the disease [73]. Healthcare providers restricting common foods generates a nutritional burden for the patient and their caregivers. It should be done only in cases where the relationship of a food with the symptoms is proven [74].

Clinical Practice Guidelines

It is difficult to determine if guidelines are regularly followed in patient treatment across LA or what, if any, standards of care are used in the region. No studies were found assessing the real-world application of current Latin American CPGs of AD. In addition, it is hard to determine whether international CPGs are commonly used instead. Application of the European Task Force on Atopic Dermatitis guidelines in a Colombian population with AD improved AD severity and QoL, and only a minority of patients achieved complete control [75].

Most information on AD from LA can be found in research articles and clinical studies by AD experts and researchers. These authors used international diagnostic and classification criteria and standard treatments recommended in local and international CPGs. Nevertheless, the findings are likely biased toward expert care and do not reflect the standard of care (SoC) received by most of the populations affected by AD.

Specifically, in terms of AD treatments, the rapid development and approval of novel therapies, both topical and systemic, leads to rapid obsolescence of multiple CPGs created even a few years earlier and causes difficulties for experts and scientific societies in publishing updated recommendations.

Guaranteed universal treatment access exists in some parts of LA, such as the Explicit Health Guarantees Law in Chile that legally guarantees universal access to diagnosis and treatment for more than 80 high-burden health problems, regardless of insurance. Unfortunately, it does not include AD.

Combating Health Disparities in AD

Few publications reference the disparities in healthcare in patients with AD in the region [62]. The Atopic Dermatitis Quality of Care (ADQoC) initiative [76] aims to develop a global vision for the standards of care for AD, create a repository of best practice interventions and their implementation, sustain collaboration with a group of experts from different countries and regions, and raise the SoC of patients with AD [76]. They surveyed 32 expert AD care centers worldwide, including hospitals in Brazil, Colombia, and Argentina [76].

The ADQoC initiative findings described barriers to achieving adequate care for patients with AD, including misconceptions about the disease, delayed referral and access to AD specialists, poor patient access to AD treatments, and poor adherence to managing the complexity of AD and its comorbidities [76]. These barriers are aggravated in LA by social inequalities and economic deficiencies. Recommendations were derived from this work to improve SoC, education of doctors and patients, access to specialists, and multidisciplinary work for the joint treatment of associated comorbidities [76].

Living Guidelines

Existing guidelines in LA are quite comprehensive, covering diagnosis, classification, outcome measures, comorbidity, and treatments. Notably, some guidelines (e.g., SLAAI) include comments on particular considerations for the region or country, indicating that local Latin American CPGs may be required to address specific epidemiologic, ethnic, and socioeconomic issues pertaining to AD diagnosis and treatments. Several treatment considerations are noteworthy: for example, the lack of coverage by many healthcare systems of moisturizers and emollient creams for AD treatment.

Some of the CPGs in LA were written before dupilumab, and other novel treatments were approved. Optimization of guideline development would allow updating individual recommendations as new evidence is discovered, creating ‘‘living guidelines’’ that can keep up with rapidly evolving treatments for AD.

Patient Education

AD is a complex problem, and its treatment can often challenge patients and HCPs. Major AD treatment guidelines currently recommend education for patients with AD [40, 41]. It is highly recommended that educational strategies be developed for the community, patients, and caregivers [76]. Different models of educational programs exist worldwide, and their structures depend on social and economic conditions. Educational programs for patients with AD can improve adherence, clinical outcomes, and QoL [77, 78]. Nonprofit organizations and medical societies exist in some countries across LA and can provide support and education for HCPs and patients (Table 2).

Table 2 Patient organizations and societies for atopic dermatitis in Latin America

Therapeutic education, a patient-centered process wherein the healthcare provider includes the patient and caregiver in treatment decision-making, has a proven valuable in chronic diseases in which treatment adherence is usually suboptimal [79]. In chronic diseases such as AD, the percentage of non-adherence to treatment ranges from 30% to 40% [80]. In some cases, this is due to corticophobia or TCS overuse and inadequate information. Therapeutic education is a way to improve adherence, empower patients, and improve QoL, and is recommended with a high level of evidence [79].

For healthcare systems, patient education reduces the demand for centers and services, providing a cost benefit to the healthcare system and decreasing the direct cost of care and the indirect cost to society [76]. Scientific societies also play an integral role in educating the general public, patients, and medical professionals (Table 2).

Leveraging Telemedicine to Advance Patients’ Access to Information and Specialists

The primary reason for the delay in referring patients to specialists is that PCPs do not recognize the condition, and it is challenging to reach experts [76]. Education is the foundation for PCPs, pediatricians, and dermatologists to understand the disease, make an accurate and timely diagnosis, and provide individualized therapy. Sociodemographic and access to information vary widely within LA and even within the same country.

Videoconferencing solutions provide both distant training for physicians and real-time or asynchronous patient access to experts. Telemedicine with videoconferencing is the practice of medicine that uses technology to provide treatment from a distance. The widespread implementation of the strategies suggested in Box 1 would assist in reducing inequities in AD care for patients living in locations where experts are few.

Box 1
figure 1

Technologies that can help equalize care. ECHO, Extension for Community Healthcare Outcomes; PCPs, Primary care physicians; HCPs, Healthcare professionals

Telementoring, successfully used in Argentina for psoriasis and AD, [81, 82] allows for the remote training of doctors. As an immediate consequence, patients can access specialists in the best available clinics without needing to travel to specialized centers. This system allows the treating physician to receive feedback while training in their local area. A mobile application developed in Argentina creates a space where patients can record symptoms, build peer-to-peer networks, schedule appointments, and communicate with their HCPs.

Socioeconomic Impact on Treatment of AD

Access to treatment is very uneven between regions, the different LA countries, and private and public healthcare systems. The development of local living CPGs [30], patient education programs that inform and empower patients, and public policies to improve the distribution of health resources are strategies that can help increase coverage of treatments for AD.

Managing Comorbidities

AD has multiple comorbidities. Multidisciplinary work is essential to carry out a holistic treatment approach: dermatologists, allergists, pediatricians, PCPs, pulmonologists, dieticians, and psychologists, among others, must work together to achieve a comprehensive care approach.

Implementing atopic and multidisciplinary clinics creates spaces that allow for the joint discussion of therapeutic alternatives, saving time for the patient and costs for the healthcare system. We must not neglect mental health since both systemic inflammation and disease burden may cause depression and ADHD.

This paper is a narrative review and thus does not include all available data, although we made every effort to find published articles on this topic. We also recognize that LA is a diverse region with varying needs of different countries and even varying needs within each country. Our panel consisted of pediatric allergists and dermatologists from six of the countries in the region, so this paper cannot address specifics to every country.

Conclusions

LA is a group of heterogeneous countries with various geographical, economical, and cultural conditions. Additionally, the organization of the healthcare system is diverse. The disparity in the access to diagnosis and treatment of AD among Latin American countries is due to factors derived from these differences. In the same country, there may be inequality between the population with higher or lower income, ethnic ancestry, or their place of residence (rural or urban area). Some of these factors can be corrected, and we propose different measures to reduce healthcare disparities in managing AD and thus achieve better disease control with a positive impact on patients and communities in LA. The accessibility to new and expensive therapies for AD, and their influence on the healthcare systems in LA, must be addressed (Fig. 1).

Fig. 1
figure 2

Barriers contributing to health disparities in atopic dermatitis and suggested actions to overcome the barriers