Abstract
Purpose of Review
Travel medicine practitioners often are confronted with returning travelers with dermatologic disorders that could be of infectious causes or inflammatory or allergic. Some dermatologic processes are the result of exposure to insects or acquired due to environmental exposures. There is a broad range of dermatosis of infectious and non-infectious etiologies that clinicians need to consider in the differential diagnosis of dermatosis in travelers
Recent Findings
With increasing international travel to tropical destinations, many individuals may be exposed to rickettsia (i.e., African tick bite fever, scrub typhus, or Mediterranean spotted fever), parasitic infections (i.e., cutaneous larva migrans, cutaneous leishmaniasis, African trypanosomiasis, or American trypanosomiasis), viral infections (i.e., measles or Zika virus infection), bacterial (i.e., Buruli ulcer) or ectoparasites (scabies or tungiasis), and myiasis. Cutaneous lesions provide clinical clues to the diagnosis of specific exposures during travel among returned travelers.
Summary
Dermatologic disorders represent the third most common health problem in returned travelers, after gastrointestinal and respiratory illness. Many of these conditions may pose a risk of severe complications if there is any delay in diagnosis. Therefore, clinicians caring for travelers need to become familiar with the most frequent infectious and non-infectious skin disorders in travelers.
Keywords: Dermatologic, Travelers, Myiasis, Tungiasis, Cutaneous Larva Migrans, Phytophotodermatitis, Prurigo Nodularis, Leishmaniasis
Introduction
The risk of travel-related illness involving the skin and soft tissues relates to an individual’s travel destination, type of itinerary, underlying medical conditions, duration of travel, level of accommodation, activities during travel, adherence to prescribed preventive medications, and environmental exposures [1••]. Among different case series, mostly of European travelers returning after traveling to the tropics, between 2 and 9% of persons experience some dermatosis during travel [1••, 2••]. After gastrointestinal and respiratory illness, skin disorders represent the third most common reason for consultation during travel or at the time of their return to their home country [2••].
This mini-review introduces the special issue of Current Tropical Medicine Reports on dermatologic conditions presenting in returning travelers with a particular focus on infectious diseases affecting skin and soft tissues. The main goal of this introductory article is to summarize the most common skin problems in travelers and a framework for developing a clinically relevant differential diagnosis.
Major Dermatologic Processes in Travelers
Cutaneous lesions provide clues to specific clinical entities which could be either strictly involving skin and soft tissues or representing dermatologic manifestations of systemic diseases [3, 4••, 5•, 6, 7]. Table 1 provides an overview of frequently identified infectious and non-infectious cutaneous disorders manifesting in returning travelers. When evaluating a patient with signs and symptoms consistent with a systemic infection, a detailed physical examination to assess skin, soft tissues, and mucosae is an important priority. Skin lesions may include a maculopapular rash, vesicular lesions, ulcerations, petechial rashes, and nodules. Viral infections manifest with papular or maculopapular rashes including dengue fever or Zika virus infection (Fig. 1). Pretibial tender nodules are consistent with erythema nodosum (Fig. 2). Many travelers experience non-infectious skin problems during travel including prurigo nodularis, photoallergic reactions (phytophotodermatitis), sunburns, and drug-related phototoxicity. Miliaria rubra (heat rash) are also clinically important in many returned travelers (Table 1) [1••, 2••, 3].
Table 1.
Summary of major dermatologic conditions in travelers
| Infectious etiologies | |
|---|---|
| Bacterial | Cellulitis (Streptococcus pyogenes, S. agalactiae, S. dysgalactiae) Folliculitis/Carbuncles (Staphylococcus aureus) Ecthyma (Pseudomonas aeruginosa or Staphylococcus aureus) Necrotizing fasciitis (Aeromonas or Streptococcus pyogenes) Eumycetoma (Nocardia brasiliensis) Verrucous lesions (Bartonella bacilliformis) Bacillary angiomatosis caused by Bartonella hensellae or Bartonella quintana (vascular lesions mimicking Kaposi’s sarcoma) Meningococcemia (petechial rash, purpura fulminans) |
| Spirochetes | Syphilis (Treponema pallidum causing chancres, condyloma latum, gummatous lesions) Pinta (hypopigmented lesions mimicking vitiligo) caused by Treponema pallidum karateum Yaws (nodules and ulcerative lesions) caused Treponema pallidum pertenue |
| Fungal | Blastomycosis (nodular, non-healing ulcers) Paracoccidioidomycosis (nodular, ulcerated lesions) Mycetoma (Madura foot) Lobomycosis (nodules in ears) Cryptococcosis (umbilicated lesions) Talaromycosis (umbilicated lesions) |
| Rickettsial | Rickettsialpox (vesicular rash after exposure to mites that feed on mice caused by R. akari) Murine typhus (maculopapular rash) Spotted fevers (eschars of Mediterranean spotted fever or African tick bite fever) Rocky Mountain spotted fever (petechial, maculopapular) Scrub typhus (exposure to chiggers transmitting Orientia tsutsugamushi) |
| Borrelial | Lyme disease (erythema migrans, lymphocytoma cutis, acrodermatitis chronic atrophicans) Tick-borne relapsing fever (maculopapular rash) |
| Viral | Exanthems (measles, rubella, dengue, chikungunya, Zika) Vesicular (chickenpox) Monkepox (exposure to prairie dogs or other rodents) Parvovirus B19 (maculopapular and arthritis) |
| Parasitic | Cutaneous and mucocutaneous leishmaniasis (multiple Leishmania spp.) Schistosomiasis (cercarial dermatitis or Katayama fever) Toxocariasis, strongyloidiasis (recurrent urticarial) Recurrent angioedema (Calabar swellings associated with the filarial Loa Loa) Chagoma and Romaña sign (swelling of the eyelid) associated with American trypanosomiasis or Chagas disease Chancre of African trypanosomiasis at the site of the Tsetse fly bite Onchocerciasis (Onchocerca volvulus nodules or onchocercoma) Ancylostoma caninum (cutaneous larva migrans) Gnathostomiasis (cutaneous larva migrans with areas of hemorrhage) Strongyloidiasis (larva currens) |
| Mycobacterial | Buruli ulcer (Mycobacterium ulcerans) Leprosy (M. leprae and M. lepromatosis) Cutaneous tuberculosis (M. tuberculosis complex) Non-tuberculous mycobacteria such as M. kansasii, M. haemophilum or rapidly growing mycobacteria: M. abscessus, M. fortuitum, M. chelonae |
| Ectoparasites | Tungiasis: Tunga penetrans Scabies: Sarcoptes scabiei |
| Myiasis | Primary Botfly: Dermatobia hominis Tumbu fly: Cordylobia anthropophaga Secondary Cochliomyia hominivorax |
| Non-infectious etiologies | |
| Phytophotodermatitis | Cutaneous phototoxic inflammatory reaction to lime/lemon/mango in the skin causing erythema and hyperpigmentation after sun exposure. May cause erythema and blisters |
| Erythema nodosum | Streptococcus pyogenes pharyngitis |
| Erythema multiforme | Herpes simplex type I or type II (initial infection or reactivation) Influenza Mycoplasma pneumoniae |
| Prurigo nodularis | Allergic reaction to insect bites which causes multiple intensely pruritic nodules in lower and upper extremities |
| Phototoxic reactions | Doxycycline Voriconazole |
| Heat rash or miliaria rubra | Heat triggers obstruction of eccrine ducts within the Malpighian layer of the skin |
| Marine exposures | Cellulitis, nodular lymphangitic spread (Mycobacterium marinum, Mycobacterium haemophilum) Necrotizing fasciitis due to Aeromonas hydrophila Cellulitis due to Edwardsiella spp., Streptococcus iniae Swimmer’s itch (cercarial dermatitis) Urticaria (aquagenic) Contact dermatitis to toxins in jelly fish |
| Miscellaneous | Exacerbation of underlying skin conditions such as acne or atopic dermatitis |
Fig. 1.
A returning traveler with a diffuse viral exanthema in patient with confirmed dengue viral infection after returning from the Peruvian Amazon
Fig. 2.
A returning traveler presenting with erythema nodosum (nodules with associated tenderness) associated to Streptococcus pyogenes pharyngitis
Bacterial Infections
Travelers may present a spectrum of clinical conditions including cellulitis to ecthyma gangrenosum (Fig. 3a, b) to necrotizing skin and soft tissue processes (Table 2). Folliculitis caused by Staphylococcus aureus, Pseudomonas aeruginosa, or rapidly growing mycobacteria is associated with travelers exposed to fresh water (i.e., Jacuzzi) [8]. Aquatic injuries in fresh water may lead to cellulitis, abscesses, or necrotizing fasciitis caused by Aeromonas hydrophila [8, 9]. Other causes of skin and soft tissue infections acquired after aquatic injuries may be caused by other bacterial pathogens including Edwardsiella tarda, Streptococcus iniae, Erysipelothrix rhusiopathiae, Mycobacterium marinum, or Vibrio vulnificus [8]. Other clinical forms of skin and soft tissue infections include nodular lymphangitic spread of infections including Staphylococcus aureus and Streptococcus spp., Nocardia brasiliensis, or non-tuberculous mycobacteria such as M. marinum or Mycobacterium haemophilum [9].
Fig. 3.
a,b Ecthyma gangrenosum caused by Staphylococcus aureus in two returning travelers
Table 2.
Common bacterial skin and soft tissue infections in travelers
| Bacterial skin and soft tissue infections | Spectrum of Illness | Mechanism of inoculation and endemic areas if applicable |
|---|---|---|
| Staphylococcal | Cellulitis, impetigo, abscess, folliculitis, furuncle, carbuncle, necrotizing fasciitis | Broken or macerated skin, traumatic inoculation |
| Streptococcal | Erysipelas, impetigo, cellulitis, necrotizing fasciitis | Broken or macerated skin, traumatic inoculation |
| Aeromonas, Edwardsiella | Cellulitis, furunculosis, necrotizing fasciitis | Injuries in freshwater, consumption of contaminated freshwater seafood—worldwide distribution |
| Vibrio vulnificus | Cellulitis, wound infection, necrotizing fasciitis | injuries in saltwater, ingestion of contaminated seafood (esp. shellfish) more often in immunocompromised hosts and those with chronic liver disease—worldwide distribution, warm coastal waters |
| Borrelia burgdorferi | Erythema migrans—early Lyme disease | Ixodes tick bite—New England, Mid Atlantic, Upper Midwest, Pacific Northwest, Europe, Japan |
| Bartonella bacilliformis | Oroya fever, verruga peruana (miliary, mular [nodular] skin lesions) | Lutzomyia verrucarum and Lutzomyia peruensis—Andean cordillera in Peru, Ecuador, Colombia, less commonly Bolivia and Chile |
| Burkholderia pseudomallei | Melioidosis, cellulitis, abscess, ulceration | Inhalation, Ingestion, Aspiration, direct skin inoculation—found in soil and water in Southeast Asia, Northern Australia, Central America, Brazil, Colombia, Venezuela, Ecuador |
| Treponema pallidum (primary, secondary syphilis) | Painless chancre at inoculation site, herpetiform ulcerations (primary syphilis), disseminated skin eruptions (follicular, lenticular, lichenoid, and annular), condyloma lata, mucous membrane lesions, lymphadenopathy (secondary syphilis), granulomatous nodules, Gumma (tertiary syphilis) | Sexual contact—worldwide |
| Mycobacterium ulcerans | Buruli ulcer (painless nodular lesion or ulceration) | Exposure of broken or macerated skin to contaminated soil or water—Africa [1••] |
| Mycobacterium marinum | Sporotrichoid nodules in lymphangitic pattern, necrotic ulcerations or plaques, nodules, verrucous lesions | Injuries in saltwater, inoculation of superficial abrasions, handling marine fish, handling or maintenance of marine aquariums |
| Nocardia brasiliensis | Actinomycetoma (chronic painless draining fistulous tract with granules) | Traumatic inoculation—worldwide in tropical and subtropical countries (between 15 degrees South and 30 degrees North latitude) |
| Actinomyces israelii | Actinomycetoma | Traumatic inoculation—worldwide in tropical and subtropical countries (between 15 degrees South and 30° North latitude) |
Fever in a returned traveler after potential tick exposure may be associated with either Rickettsia spp., Borrelia spp., or Francisella tularensis. Some tick-borne illness produce eschars (tache noire of African tick bit fever, or Mediterranean spotted fever) or maculopapular disseminated rashes [3]. Lyme disease manifest as erythema migrans during early infection [10]. Travelers who acquire Lyme disease in Europe caused by Borrelia afzelii or Borrelia garinii may lead to lymphocytoma cutis, acrodermatitis chronica atrophicans, or morphea type lesions [11••, 12•].
Parasitic Infections Manifesting in Travelers
Cutaneous Leishmaniasis
Cutaneous leishmaniasis (Fig. 4) is the most frequently reported form of leishmaniasis after visceral and mucocutaneous forms [13]. Exposure to sandflies in some settings may cause cutaneous leishmaniasis and may be associated with more than 20 Leishmania species with different degrees of pathogenicity. Clinically, leishmaniasis manifests as a non-healing ulcerative lesions (Fig. 5), nodular lesions, and atypical presentations including verrucous, sporotrichoid, or impetiginous forms (Figs. 6 and 7a, b).
Fig. 4.
Cutaneous leishmaniasis due to Leishmania panamensis
Fig. 5.
Cutaneous leishmaniasis due to Leishmania panamensis in the hand of a returning traveler.
Fig. 6.
Cutaneous Leishmaniasis (Tapir Nose)
Fig. 7.
a,b Cutaneous Leishmaniasis (Úlcera de chiclero)
Cutaneous Larva Migrans
This cutaneous parasitic infection occurs in travelers walking barefoot in sand beaches in the tropics. It manifests a few days after the initial inoculation site as creeping dermatitis or eruption. Most presentations occur as linear or serpiginous skin eruption associated with pruritus (Fig. 8). Larvae of specific nematodes penetrate the skin as in the case of Ancylostoma caninum or Ancylostoma braziliense. Other forms of cutaneous larva migrans are associated with Gnathostoma spp. after oral ingestion or contaminated fish. Due to incomplete larval development of specific nematodes, the human host reacts inflammation surrounding the larval tract in the affected cutaneous site. Treatment involves the use of a short course of antiparasitic therapy with either albendazole or ivermectin.
Fig. 8.
A returning traveler with cutaneous larva migrans in her left foot sole presenting after returning from southeast tropical Asia
Infestations: Myiasis and Tungiasis
Myiasis is a common dermatologic infection in returning travelers, accounting for nearly 10% of all travel related dermatologic infections [3, 14, 15]. Myiasis occurs when a human being plays host to insect larvae, frequently, but not exclusively, from the Calyptratae subsection of the Diptera order (Table 3). Often associated with travelers returning from the Central and South America and Sub-Saharan Africa, there are potentially pathogenic dipteran flies on every continent except Antarctica. Infestation is typically conceptualized as primary or secondary myiasis [3, 14]. In primary myiasis, larvae penetrate otherwise healthy skin and can manifest as either furuncular or migratory infection. Secondary myiasis involves infestation of broken skin, commonly open wounds or ulcerating or fungating malignancy, or infestation of a body cavity as in aural, nasal, or orbital myiasis. Furuncular myiasis typically begins as a nodule or papule with central punctum through which the larva breathes and excretes waste and can be associated with pain, erythema, discharge, and the sensation of movement. Migratory myiasis occurs when fly larvae find themselves in humans as an accidental host, resulting in a meandering pattern of erythema that follows the subcutaneous path of the migratory larvae [3, 14] (Fig. 8). Treatment for all forms of myiasis involves expression or excision of the Diptera larvae from the patient by promoting larval attempting to escape through the respiratory pore where the larva obtains oxygen [15, 16].
Table 3.
Primary and secondary forms of myiasis in travelers
| Dermatobia hominis | Furuncular myiasis | Central and South America |
|---|---|---|
| Cordylobia anthropophaga | Furuncular myiasis | Sub-Saharan Africa |
| Cordylobia rodhaini | Furuncular myiasis | Africa |
| Cuterebra spp. | Furuncular myiasis, visceral infestation, respiratory tract infestation | North America |
| Wohlfahrtia vigil | Furuncular myiasis | North America, Europe, Asia |
| Wohlfahrtia magnifica | Furuncular myiasis, secondary myiasis | Mediterranean region, North Africa, Southern Europe, East Asia |
| Cochliomyia hominivorax | Secondary myiasis | Latin America |
| Gasterophilus intestinalis | Migratory myiasis | Worldwide |
Figure 9 shows Dermatobia hominis extracted from a cutaneous nodule on the back of a male patient. Tungiasis, also known as nigua, is an infestation of soft tissues caused by the female sand flea Tunga penetrans that usually manifests in the lower extremities [16]. Management requires mechanical extraction of the larva [17]. This condition may complicate with secondary infection leading to cellulitis and osteomyelitis (Fig. 10). Lice infestations may lead to systemic illnesses such as relapsing fever or Bartonella quintana endocarditis (trench fever) [18–22].
Fig. 9.
Larval form of Dermatobia hominis extracted from a cutaneous nodule on the back of a returning traveler
Fig. 10.
A returning traveler from South America with tungiasis caused by Tunga penetrans
Conclusions
Febrile or non-febrile conditions presenting in returned travelers often involve the skin and soft tissues. Cutaneous lesions may constitute a localized systemic infection or cutaneous manifestations of systemic infections. Along with obtaining a specific travel itinerary and history of environmental exposures, a detailed examination of skin and soft tissues is central in searching for specific skin lesions that represent clues to specific etiologies in travelers.
Footnotes
Conflict of Interest All authors declare that they have no conflict of interest.
Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.
References
Papers of particular interest, published recently, have been highlighted as:
• Of importance
•• Of major importance
- 1.••.Hochedez P, Caumes E. Common skin infections in travelers. J Travel Med. 2008;15(4):252–62 [DOI] [PubMed] [Google Scholar]; This is a classic article written by dermatologist with extensive experience and expertise in travel medicine which provides a detailed description of dermatologic conditions in travelers.
- 2.••.Wilson ME, Chen LH. Dermatologic infectious diseases in international travelers. Curr Infect Dis Rep. 2004;6:54–62 [DOI] [PubMed] [Google Scholar]; In depth narrative review of dermatologic conditions in travelers.
- 3.Francesconi F, Lupi O. Myiasis. Clin Microbiol Rev. 2012;25(1):79–105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.••.Reis CMS, Reis-Filho EGM. Mycetomas: an epidemiological, etiological, clinical, laboratory and therapeutic review. An Bras Dermatol. 2018;93(1):8–18 [DOI] [PMC free article] [PubMed] [Google Scholar]; Narrative review of mycetoma and actinomycetoma.
- 5.•.Jensenius M, Fournier PE, Raoult D. Rickettsioses and the international traveler. Clin Infect Dis. 2004;39(10):1493–9. 10.1086/425365 [DOI] [PubMed] [Google Scholar]; Comprehensive review of clinically relevant Rickettsial infections in travelers including African tick bite fever and Mediterranean spotted fever.
- 6.Raff AB, Kroshinsky D. Cellulitis: a review. JAMA. 2016;316(3):325–37. [DOI] [PubMed] [Google Scholar]
- 7.Franco-Paredes C, Chastain DB, Allen L, Henao-Martínez AF. Overview of cutaneous mycobacterial infections. Current Tropical Medicine Reports. 2018;5(4):228–32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Horseman MA, Surani S. A comprehensive review of Vibrio vulnificus: an important cause of severe sepsis and skin and soft-tissue infection. Int J Infect Dis. 2011;15(3):e157–66. [DOI] [PubMed] [Google Scholar]
- 9.Goncalves Pessoa RB, de Oliveira WF, Marques DSC, Dos Santos Correia MT, de Carvalho E, Coelho L. The genus Aeromonas: a general approach. Microb Pathog. 2019;130:81–94. [DOI] [PubMed] [Google Scholar]
- 10.Nadelman RB. Erythema migrans. Infect Dis Clin North Am. 2015;29(2):211–39. [DOI] [PubMed] [Google Scholar]
- 11.••.Malane MS, Grant-Kels JM, Feder HM Jr, Luger SW. Diagnosis of Lyme disease based on dermatologic manifestations. Ann Intern Med. 1991;114(6):490–8 [DOI] [PubMed] [Google Scholar]; This article provides the most relevant clinical description of the dermatologic manifestations of Lyme disease.
- 12.•.Godar DA, Laniosz V, Wetter DA. Lyme disease update for the general dermatologist. Am J Clin Dermatol. 2015;16(1):5–18 [DOI] [PubMed] [Google Scholar]; This article raised awareness of the importance of rickettsioses in international travelers.
- 13.Franco-Paredes C The growing challenge of leishmaniasis in travelers. Travel Med Infect Dis. 2014;12(6 Pt A):559–60. [DOI] [PubMed] [Google Scholar]
- 14.Center for Disease Control and Prevention (CDC). Myiasis. https://www.cdc.gov/dpdx/myiasis/index.html. Published 2020. Accessed11/29/2020.
- 15.Osorio J, Moncada L, Molano A, Valderrama S, Gualtero S, Franco-Paredes C. Role of ivermectin in the treatment of severe orbital myiasis due to Cochliomyia hominivorax. Clin Infect Dis. 2006;43(6):e57–9. [DOI] [PubMed] [Google Scholar]
- 16.Cestari TF, Pessato S, Ramos-e-Silva M. Tungiasis and myiasis. Clin Dermatol. 2007;25(2):158–64. [DOI] [PubMed] [Google Scholar]
- 17.Coates SJ, Thomas C, Chosidow O, Engelman D, Chang AY. Ectoparasites: pediculosis and tungiasis. J Am Acad Dermatol. 2020;82(3):551–69. [DOI] [PubMed] [Google Scholar]
- 18.Stevens DL, Bryant AE. Necrotizing soft-tissue infections. N Engl J Med. 2017;377(23):2253–65. [DOI] [PubMed] [Google Scholar]
- 19.Sanchez Clemente N, Ugarte-Gil CA, Solorzano N, et al. Bartonella bacilliformis: a systematic review of the literature to guide the research agenda for elimination. PLoS Negl Trop Dis. 2012;6(10):e1819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol. 2006;4(4):272–82. [DOI] [PubMed] [Google Scholar]
- 21.Tellez I, Franco-Paredes C. A woman with chronic subcutaneous swelling of the right foot associated with sinus tracts discharging yellow grains. PLoS Negl Trop Dis. 2010September28;4(9):e772. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Lautenschlager S Cutaneous manifestations of syphilis. American Journal of Clinical Dermatology. 2006;7:291–304. [DOI] [PubMed] [Google Scholar]