Skin diseases in the Peruvian Amazonia

Tropical medicine rounds Skin diseases in the Peruvian Amazonia Ericson L. Gutierrez1, MD, Carlos Galarza1, MD, Willy Ramos1, MD, Mercedes Tello1, BSc, Gerardo Jiménez2, MD, Gerardo Ronceros1, MD, Humberto Chı́a3, MD, Jorge Hurtado1, MD, and Alex G. Ortega-Loayza4, MD 1 Instituto de Investigaciones Clı́nicas, Universidad Nacional Mayor de San Marcos (UNMSM), Lima, Perú, 2 Servicio de Dermatologı́a, Hospital Regional de Pucallpa. Pucallpa, Ucayali, Perú, 3Servicio de Dermatologı́a de la Universidad Nacional Mayor de San Marcos (UNMSM), Lima, Perú, and 4 Department of Internal Medicine, Virginia Commonwealth University, Richmond, VA, USA Abstract Background Dermatologic diseases vary widely as a result of geographic location and may be influenced by environmental factors. Aim To determine the epidemiology of dermatological diseases in the Peruvian Amazonia. Methods Transversal and multicentric study, which were carried out during February of 2006, 2007, and 2008 in three regional hospitals in the Peruvian Amazonia. All new patients who were looking for dermatological consultation were included. Univariate/ bivariate analysis, chi square, and multinomial logistic regression were used with a confidence level of 95%. Results A total of 1602 patients were included. The infectious and parasitic dermatoses were the most prevalent (31.5%). There was a statiscally significant association between Correspondence Alex G. Ortega-Loayza, MD Department of Internal Medicine, Virginia Commonwealth University, PO Box 980509, Richmond, VA 23298-0509, USA E-mail: [email protected] There is no financial conflict with the subject materials or materials discussed in the manuscript. We have no relevant financial interest in this manuscript. infections of the skin and subcutaneous tissue in children (P < 0.001). The parasitic dermatoses such as scabiosis, pediculosis, and myiasis were associated with an altitude less than 700 meters above sea level (m.a.s.l.) (P = 0.003, OR = 3.1, CI: 1.5–6.7). On the other hand, radiation-related disorders of the skin and subcutaneous tissue were associated with more than 700 m.a.s.l. (P < 0.01, OR = 2.9, CI: 1.7–4.9). Conclusions Infectious dermatological diseases were the most common diagnoses in the Peruvian Amazonia. In addition, radiation-related disorders of the skin should be addressed for people living/traveling in the rainforest area. These findings may assist in the training of general doctors in diagnosis and treatment of the most common dermatoses in tropical areas. Moreover, this study would be helpful for physicians from developed countries when giving medical advice/attention to travelers or immigrants of tropical areas. Introduction 794 Dermatologic diseases vary widely as a result of geographic location and they may be influenced by ethnic and environmental factors. Moreover, they are an important cause of morbidity, economic burden, and social exclusion. In developing countries, dermatological diseases are a remarkable problem in public health, especially those with infectious etiology.1 Therefore, they are considered in the Disease Control Priorities Project of the World Bank/WHO/Fogarty International Center.2 Additionally, the exponential increase of tourist activity in Peru has created a serious health risk due to the popularity of jungle destinations.3 Some studies demonstrate that approximately 8% of travelers who come back from tropical areas feel sick enough to seek medical attention.4 Dermatological diseases are one of the main causes of morbidity in South America. Leishmaniasis and miasis are the most common dermatoses affecting travelers.4,5 International Journal of Dermatology 2010, 49, 794–800 The Peruvian Jungle is greater than half of the country and it is the second largest jungle after the Brazilian Amazonia. The area of this study was represented by three locations and covered the two eco-regions of the Peruvian jungle (Fig. 1): Highland Jungle (Huanuco) and Lowland Jungle (Tingo Maria and Pucallpa). The limit between both is an altitude of 700 meters above sea level (m.a.s.l.). The main differences are the higher mean temperatures and the annual rainfall in the Lowland Jungle6 (Table 1). In these regions, people are principally mixed race with low income per family. The infection of the skin and subcutaneous tissue with superficial mycosis are the main reasons of dermatological consultation and have a similar distribution in these three different locations;7 however, there is no additional information about the main types of dermatoses in this area. The aim of this study was to determine the prevalence of dermatological diseases in three different regional hospitals of the Peruvian Amazonia and to identify risk factors for dermatologic diseases. ª 2010 The International Society of Dermatology Gutierrez et al. Skin diseases in the Peruvian Amazonia Tropical medicine rounds into different groups based on the International Classification of Diseases (ICD-10). For data entry and statistical analysis, SPSS version 15.0 (SPSS Inc., Chicago, IL, USA) was used, consisting of univariate, bivariate, and multivariate analysis. For the multivariable analysis, a model of multinomial logistic regression was used adjusting age, gender, and the altitude of the studied communities. All the calculations were made with a confidence interval (CI) of 95%. Results Figure 1 Area where the study was performed: (1) Highland Jungle; (2) and (3) Lowland Jungle Patients and methods A descriptive, cross-sectional, and multicenter study carried out in February of 2006, 2007, and 2008 at three different regional hospitals: Huanuco (Highland Jungle) and Tingo Maria and Pucallpa (Lowland Jungle). All new patients who were looking for dermatological attention were included. Diagnoses were based on single clinician’s criteria and skin biopsy as well as direct smear when needed. The dermatologic diagnosis, gender, age, and origin were recorded for each patient. Patients who were referred for different skin problems were considered as separate cases. The diagnoses were classified Table 1 Geographic characteristics of the study area Huanucoa Tingo Mariab Pucallpab A total of 1602 patients were included in this study, the mean age was 28.3 ± 21.4 years old, 52.9% were women and 47.1% were men. The main group of age was <15 years old (31%) followed by the 16–30 years old group (30.6%), 31–45 years old (14.6%), 46–60 years old (11.9%), 61–75 years old (6.5%), and >75 years old (5.3%). By group of disease, the infectious and parasitic dermatoses, including the infections of skin and subcutaneous tissue, were the most common (31.5%), followed by dermatitis (26.9%), and diseases of skin appendages (11.4%). The distribution of dermatological diseases is in Table 2. By disease, the dermatophytosis was the most prevalent diagnosis (8.4%), followed by allergic contact dermatitis (6.7%), facial melanosis (5.7%), and acne (5.5%) (Table 2). The most frequent endemic dermatoses was cutaneous leishmaniasis (2.5%) followed by classical dengue (0.9%), leprosy (0.4%), and endemic pemphigus foliaceus (0.4%) (Table 3). The clinical characteristics of patients with leprosy are described in Table 4. We found a statistically significant association between the diseases of skin appendages (P = 0.030), benign neoplasms (P = 0.040), radiation-related disorders of the skin and subcutaneous tissue (P = 0.023), vitiligo and facial melanosis (P < 0.001) with the patients’ gender. Also, we found a statistically significant association between dermatitis (P = 0.007), diseases of skin appendages (P = 0.040), vitiligo and facial melanosis (P = 0.030), infections of the skin and subcutaneous tissue (P < 0.001), malignant neoplasms (P < 0.001) and 32 Number of patients Longitude (W) Latitude (S) Altitude (m.a.s.l) Mean annual temperature (°C) Mean population Annual rainfall (mm) 800 302 500 76°14¢ 75°59¢ 74°31¢ 9°55¢ 9°17¢ 8°22¢ 1500 672 154 19 22 24 122 098 18 000 200 000 396 3300 1570 a Highland Jungle, bLowland Jungle. ª 2010 The International Society of Dermatology International Journal of Dermatology 2010, 49, 794–800 795 796 Tropical medicine rounds Skin diseases in the Peruvian Amazonia Table 2 Main skin diseases diagnoses in three localities of Gutierrez et al. Table 2 Continued the Peruvian Amazonia Diseases Diseases Other bacterial diseases Leprosy [Hansen’s disease] Tuberculosis of skin and subcutaneous tissue Cutaneous bartonellosis [Verruga peruana] Infections with a predominantly sexual mode of transmission Chlamydial lymphogranuloma [venereum] Urogenital trichomoniasis Herpesviral infection of genitalia Viral infections Viral warts Classical dengue Herpesviral vesicular dermatitis Mycoses Dermatophytosis Onychomycosis Pityriasis versicolor Protozoal diseases Cutaneous leishmaniasis Infestations Scabies Pediculosis and phthiriasis Cutaneous myiasis Infections of the skin and subcutaneous tissue Cutaneous abscess, furuncle and carbuncle Impetigo Other local infections of skin and subcutaneous tissue Benign neoplasms Other benign neoplasms of skin Melanocytic nevi Malignant neoplasms Basal cell carcinoma Squamous cell carcinoma Melanoma Bullous disorders Endemic pemphigus foliaceus Pemphigus vulgaris Pemphigoid Dermatitis Allergic contact dermatitis Pityriasis alba Atopic dermatitis Other dermatitis Papulosquamous disorders Psoriasis Other papulosquamous disorders Pityriasis rosea Urticaria and erythema Urticaria Other erythematous conditions Radiation-related disorders of the skin and subcutaneous tissue Other acute skin changes because of ultraviolet radiation Actinic keratosis Patients 10 7 1 1 4 0.6 0.4 0.1 0.1 0.2 1 1 1 89 53 15 13 227 134 40 36 40 40 55 52 2 1 83 39 0.1 0.1 0.1 5.6 3.3 0.9 0.8 14.2 8.4 2.5 2.2 2.5 2.5 3.4 3.2 0.1 0.1 5.2 2.4 23 14 1.4 0.9 71 43 28 17 11 5 1 11 7 1 1 431 107 80 64 180 64 26 20 15 52 42 10 62 4.4 2.7 1.7 1.0 0.7 0.2 0.1 0.6 0.4 0.1 0.1 26.9 6.7 5.0 4.0 11.2 4.0 1.6 1.2 0.9 3.2 2.6 0.6 3.9 32 2.0 27 1.7 International Journal of Dermatology 2010, 49, 794–800 Patients % % Disorders of skin appendages Acne Rosacea Miliaria rubra Other disorders of the skin and subcutaneous tissue Facial melanosis Vitiligo Seborrhoeic keratosis Total 182 88 25 25 204 11.4 5.5 1.6 1.6 12.5 92 31 11 1602 5.7 1.9 0.7 100.0 radiation-related disorders of the skin and subcutaneous tissue (P = 0.002) with the group’s age (Table 5). The two eco-regions of the Peruvian Amazonia showed different statistically significant associations with dermatological diseases. In the Highland Jungle (Huanuco) radiation-related disorders of the skin and subcutaneous tissue (P < 0.001), pityriasis alba (P = 0.014), acne (P < 0.001), and atopic dermatitis (P = 0.002) were most prevalent, while in the Lowland Jungle (Tingo Maria and Pucallpa) infestations (P = 0.003) (Table 6) were the dominate diagnoses. Discussion Infectious dermatological diseases were the most common diagnoses in the Peruvian Amazonia, which has similar climatic conditions with other tropical regions worldwide. The confluence of environmental factors such as vegetation, topographic conditions, presence of lakes, rivers and collections of water in the Peruvian jungle could explain the high percentage of dermatological diseases which have had an infectious origin (31.5%).8 Similar results have been obtained in Hormozgan/Irán (31%)9 and also in Hajjah/Yemen (24.2%).10 This is different in countries of Africa where the percentage of infectious dermatoses is higher with 41% in Bamako (Mali),11 44.4% in Sokoto (Nigeria)12 and 46% in Kumasi (Ghana).12 Superficial mycoses were the main diagnosis in our study, probably because of the presence of humidity and heat trigger proliferation of dermatophytes fungi and species of Malassezia.14 Similar results were found in regions of Yemen10 and Iran.9 Scabiosis is a parasitic dermatosis that is common in tropical areas1 and represented 3.2% in our study. Poor sanitary conditions, crowding, and malnutrition created the appearance of scabiosis in this area. Impetigo, cutaneous abscess, furuncle, carbuncle, cellulites, and other superficial skin infections represented 5.2% and appeared ª 2010 The International Society of Dermatology Gutierrez et al. Skin diseases in the Peruvian Amazonia Tropical medicine rounds Table 3 Endemic skin diseases diagnoses in three locations of the Peruvian Amazonia Age-stratified groups Gender Procedence Diseases 0–15 16–30 31–45 45–60 61–75 M F H TM P Total (%) Cutaneous leishmaniasis Classical dengue Leprosy Endemic pemphigus foliaceus Sporotrichosis Cutaneous bartonellosis [Verruga peruana] Paracoccidiomycosis Chromomycosis Cutaneous myiasis 2 1 1 – 1 1 17 10 – 3 – – 15 2 3 1 – – 4 2 3 – 1 – 2 – – 2 – – 30 10 6 5 1 1 10 5 1 1 1 – 10 – – – – – 3 – – – – 1 27 15 7 6 2 – 40 15 7 6 2 1 1 1 1 – – – – – – – – – – – – 1 1 1 – – – – – – 1 – – – 1 1 (2.5) (0.9) (0.4) (0.4) (0.1) (0.1) 1 (0.1) 1 (0.1) 1 (0.1) H, Huánuco; TM, Tingo María; P, Pucallpa. Table 4 Clinical characteristics of patients with leprosy Age Gender Ridley–Jopling scale WHO classification Disability degree 10 48 58 34 40 54 44 F M M M M M M Lepromatose Lepromatose Tuberculoid Borderline Lepromatose Lepromatose Lepromatose Multibacillary Multibacillary Paucibacillary Multibacillary Multibacillary Multibacillary Multibacillary Without disability Without disability Without disability Disability degree II: mild deformity Without disability Disability degree I: anesthesia Without disability WHO, World Health Organization. Table 5 Skin diseases by gender and age Gender Age-stratified groups Male Adult (16–60) Children (0–15) Female Older (>60) Disease n % n % n % n % n % Total Dermatitis Superficial mycoses Disorders of skin appendages Vitiligo and facial melanosis Viral infections Infections of the skin and subcutaneous tissue Benign neoplasms Papulosquamous disorders Radiation-related disorders of the skin and subcutaneous tissue Infestations Urticaria and erythema Malignant neoplasms 184 95 59 25 35 39 11.5 5.9 3.7 1.6 2.2 2.4 247 115 123* 98** 54 44 15.4 7.2 7.7 6.1 3.4 2.7 171 75 61 12 23 51** 10.6 4.7 3.8 0.7 1.4 3.2 225** 131 121* 105* 63 26 14.0 8.2 7.5 6.6 3.9 1.6 36 4 0 6 3 6 2.2 0.3 0.0 0.4 0.2 0.4 431 210 182 123 89 83 15 24 16 0.9 1.5 1.0 56* 40 46* 3.5 2.5 2.9 36 15 3 2.2 0.9 0.2 36 45 48* 2.2 2.8 3.0 0 4 10 0.0 0.3 0.6 71 64 62 27 24 7 1.7 1.5 0.4 28 28 10 1.7 1.7 0.6 26 15 0 1.6 1.0 0.0 25 35 9 1.6 2.2 0.6 4 1 8* 0.2 0.1 0.5 55 52 17 v2: *P < 0.05;**P < 0.01. ª 2010 The International Society of Dermatology International Journal of Dermatology 2010, 49, 794–800 797 798 Tropical medicine rounds Skin diseases in the Peruvian Amazonia Table 6 Skin diseases by geographic location Eco-regions/asociated diseases Highland Jungle (Huanuco) Radiation-related disorders of the skin and subcutaneous tissue Facial melanosis Pityriasis alba Acne Atopic dermatitis Lowland Jungle (Tingo Maria and Pucallpa) Infestations P-value ORa/CI <0.001 2.9 [1.7–4.9] <0.001 0.014 <0.001 0.002 2.8 1.7 2.5 2.2 0.003 [1.8–4.4] [1.1–2.7] [1.6–4.0] [1.3–3.7] 3.1 [1.5–6.7] a OR adjusted by gender and age. especially in children. A low socioeconomic level and improper hygiene in combination with hot weather increases these types of infections. Dermatitis represented the second group of the most common diseases in our study (26.9%) and appeared especially in adults coinciding with findings in Hormozgan (Irán)9 and Hajjah (Yemen)10 and being greater than in countries of Africa.11–13 In this group, allergic contact dermatitis is the most common diagnosis. This dermatitis varies considerably in accordance with the population and the area.15 Moreover, previous studies demonstrated that many species of plants produce environmental allergens which could induce appearance of this disease16 because of abundance of vegetation in the Peruvian jungle. Disorders of skin appendages, presenting with greater frequency in younger women, are the next group of diseases generally diagnosed (11%). Acne was the most common consultation. Disorders of pigmentation such as facial melanosis and vitiligo are the next group in frequency in our study (7.6%). The chronic exposure to intense solar radiation without any protection could explain the high percentage of facial melanosis (5.7%)17 and its greater frequency in younger women could be related to the use of make up and common visitation to specialists for esthetic reasons.18 Cutaneous neoplasms represented the main reason of consultation in developed countries,19 decreasing their frequency in developing countries. In our study benign neoplasms represented 4.4%, and appeared especially in women coinciding with findings in the Northeast of Nigeria,12 and being higher in others regions of Africa10,12 and the Middle East.9,10 Malignant neoplasms represented a low percentage (1%). The main diagnosis was basal cell carcinoma and its frequency was significantly higher in older people, coinciding with findings in others cities of the Peruvian coast.20 Psoriasis presents especially in countries of the northern hemisphere and decreases its incidence in tropical areas.21 International Journal of Dermatology 2010, 49, 794–800 Gutierrez et al. On the contrary, in our study, psoriasis represented 1.6% of medical consultations which were greater than the values found in the Mediterranean island of Heraklion (Greece),22 where it represented 1.2% of medical treatment during 2003. Endemic dermatoses represented a public health problem in tropical areas of Peru. In our study, the main diagnosis was cutaneous leishmaniasis. In Peru, this dermatosis is mostly because of Leishmania peruviana, affecting principally children, and is the most common clinical type described between latitudes 5ªS and 13ªS.23 Cutaneous leishmaniasis is mainly endemic not only in valleys of the Highland Jungle23 but also it has been reported previously in the Lowland Jungle.24 Therefore, inhabitants and visitors are at risk of contracting the infection. Patients with classical dengue were also seen for dermatological reasons and they presented a maculopapular erythematous rash. In our country, leprosy is in eradication process. In 2008, 37 new cases were reported, being 35 new cases per year as average during the past several years. The incidence that have been estimated is less than 1/10 000 inhabitants. The areas where leprosy was reported were Ucayali (Pucallpa), Loreto, San Martin, and Amazonas. In Huanuco, a previous endemic area, there were no cases of leprosy reported in the past couple of years. In our study, we have only found cases of leprosy in Pucallpa: two new patients in 2006 and 2007 respectively, and three new patients in 2008. The treatment is free of cost and provided only in one hospital in the area. There are no mobile or small clinics where treatment is provided. Therefore, patients have to come to the main hospital to receive their therapy. There is a chance that some patients might have leprosy in the area but they are not seeking or receiving medical attention.25 Endemic pemphigus foliaceus (EPF) represented 0.4% of patients and it has been studied in endemic areas of the Peruvian jungle. Recently Galarza et al. (2006) established the clinical, epidemiological and immunopathologic profile of EPF in Peru, determining endemic areas in Ucayali, Loreto, Huánuco, Junín, Amazonas, and San Martín.26 Also, two highlighting diagnoses were the presence of a patient with pemphigus vulgaris and another with pemphigoid, both from an endemic area of EPF (Pueblo Libre Community situated 34 km from Pucallpa/ 8°29¢45¢¢S latitude and 75°48¢00¢¢W longitude). Recently, in our country, it has been suggested the possible endemicity of bullous disorders different to EPF,27 coinciding with the findings in Brazil.28 Other endemic dermatoses found were sporotrichosis, cutaneous bartonellosis [Verruga peruana], ª 2010 The International Society of Dermatology Gutierrez et al. paracoccidiomycosis, chromomycosis, and cutaneous myiasis. Despite the low frequency of these diagnoses in this study, their importance is not decreased. These findings suggest that geographic and environmental differences between the two eco-regions of the Peruvian jungle influence the presentation of dermatological diseases. Therefore, despite the mean lower temperature in the Highland Jungle (Huanuco), there were more frequent diseases related with solar exposure as radiation-related disorders of the skin and subcutaneous tissue, pityriasis alba and facial melanosis. It is known that at a high altitude, the percentage of UV radiation penetrating the atmosphere is greater,29 and in this population, that would be the main trigger factor for radiation-related diseases. In the Highland Jungle, we also appreciated an increase in the frequency of acne, although in accordance with the previous examples, we would expect the contrary because of U.V. radiation induced inhibition of pathogenic bacteria and reduced excretion of grease,30 so, in this case, the lowest temperature plays a more important role in the appearance of this disease. Extensibility, hydration, and resistance of the stratum corneum of epidermis are reduced when the temperature is low. This could explain the high number of patients with atopic dermatitis in the Highland Jungle.31 In the Lowland Jungle, infestations were more frequent, most likely because of the high temperatures and larger populations contributing to the proliferation of ectoparasites. This study shows a general view of the main dermatoses in the Peruvian jungle, and how those could vary in accordance to environmental factors. These findings may assist in the training of general doctors in diagnosis and treatment of the most common dermatoses in tropical areas. This is especially relevant in regards to the physicians’ shortage in the Amazonia region. Because of the shortage of dermatologists in the Peruvian Amazonia, the findings presented in this study could help the sanitary authorities to train general physicians in the examination and diagnosis of most common dermatoses in this area. In addition, this study could help foreign dermatologists in the prevention and diagnosis in travelers or immigrants from these areas. Skin lesions may be useful clues to systemic/localized diseases in immigrants, short-term, and long-term residents. Acknowledgments Maybbe Mendoza, Rosario Macetas and Alfonso Gomez who contributed in the medical attention of patients. This work was supported in part by Unidad de Investigación of the Facultad de Medicina de la Universidad Nacional Mayor de San Marcos (San Fernando) and Consejo Supeª 2010 The International Society of Dermatology Skin diseases in the Peruvian Amazonia Tropical medicine rounds rior de Investigación of the Universidad Nacional Mayor de San Marcos (Lima, Peru). 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