- Email: [email protected]
A survey of plants responsible for causing allergic contact dermatitis in the Amathole District, Eastern Cape, South Africa
South African Journal of Botany 97 (2015) 32–39
Contents lists available at ScienceDirect
South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb
A survey of plants responsible for causing allergic contact dermatitis in the Amathole District, Eastern Cape, South Africa Wilfred Mbeng Otang 1, Donald Scott Grierson 2, Anthony Jide Afolayan ⁎ MPED Research Centre, Department of Botany, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa
a r t i c l e
i n f o
Article history: Received 6 November 2014 Received in revised form 8 December 2014 Accepted 23 December 2014 Available online 14 January 2015 Edited by J Van Staden Keywords: Survey Allergic contact dermatitis Eastern Cape, South Africa
a b s t r a c t Background: An inventory of allergenic plants can enable vulnerable individuals to discover the source of their dermatitis and thus prevent re-exposure. However, because of the relatively little data available in the scientific literature with regard to the adverse effects of plant, the aim of this study was to document the plants responsible for allergic contact dermatitis (ACD) in the Eastern Cape. Interview questions targeted the local names of plants that cause allergies when in direct contact with the skin. Results: Twenty four plant species in 11 families were reported as causative agents of ACD. The Asteraceae was probably the most important allergenic plant family, represented by commonly used medicinal plants such as Artemisia afra, vegetables such as Lactuca sativa and weeds such as Conyza bonariensis. Sub-acute eczematous lesions of the face and the exposed areas of the upper limbs were characteristic of Asteraceae allergies. Out of the 24 plants mentioned for causing ACD, 67% are principally used as food. Conclusions: A high burden of occupational skin disease in the food industry will definitely translate into large costs in terms of days lost from work and adjustments necessary in the workplace. Therefore, health care practitioners need to be aware of possible occupational causes for all cases of ACD. © 2015 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction The skin is the largest organ of the human body. As the outermost barrier of the human body, it is the first to encounter chemical and physical factors from the environment and therefore prone to many health problems. Numerous occupations are associated with the risk of developing reactions to plants. These include food handlers, caterers, market gardeners, farmers, agricultural workers, florists, nursery workers, landscapers, forestry workers and loggers. It is estimated that 50% of agricultural occupational skin disease is due to plants, trees and natural vegetation (Modi et al., 2009). Plants can harm the skin in numerous ways: irritant contact dermatitis due to mechanical injury or by irritant chemicals in the plant sap, phytophotodermatitis resulting from skin contamination by plants containing furocoumarins following subsequent exposure to UV light and immediate (type I) or delayed hypersensitivity contact reactions mediated by the immune system in individuals sensitised to plants or plant products e.g. peanut allergy and poison ivy poisoning (van Ketel, 1975). Dermatitis and eczema are used synonymously to denote a polymorphous pattern of skin inflammation characterised at least in its acute phase by erythema,
⁎ Corresponding author. Tel.: +27 406022323; fax: +27 86 628 2295. E-mail addresses: [email protected] (W.M. Otang), [email protected] (D.S. Grierson), [email protected] (A.J. Afolayan). 1 Tel.: +27 33257274; fax: +27 866282409. 2 Tel.: +27 406022321; fax: +27 866282409.
http://dx.doi.org/10.1016/j.sajb.2014.12.006 0254-6299/© 2015 SAAB. Published by Elsevier B.V. All rights reserved.
vesiculation and pruritus (Saint-Mezard et al., 2004) while an allergy is an immune reaction causing local or systemic acute inflammation in susceptible individuals after repeated exposure to certain antigens. Approximately one third of people will suffer from an allergy at some time in their lives and 15–20% of children suffer from atopic eczema (Ben-Shoshan et al., 2012). Allergic contact dermatitis (ACD) is a T-cell-mediated inflammatory reaction of the skin that occurs in sensitised individuals (Modi et al., 2009). ACD requires the activation of antigen-specific acquired immunity leading to the development of effector T cells which mediate the inflammation. It is characterised by redness, papules and vesicles, followed by scaling and dry skin. Unlike irritant dermatitis, allergic contact dermatitis requires previous sensitisation to the allergen and a sensitised immune system; hence, not everyone will develop an allergy to a culprit compound (Sasseville, 1999). The Eastern Cape Province of South Africa is particularly known for its richness in plant species (Phillipson, 1987). The Xhosas, who are the major inhabitants of this province had no interaction with the Western world for many years, hence, they relied mainly on traditional knowledge of medicinal plants for the treatment of various diseases and ailments. The daily activities of the Xhosa people are centred mainly on agriculture: cattle rearing and the production of crops and vegetables in small fields along the rivers and in home gardens (Bhat and Jacobs, 1985). In addition to agriculture the gathering of wild fruits and other edible plant parts, the collection of honey and the hunting of wildlife also contribute to their livelihood. This high interaction with plants on
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
a daily basis may theoretically result in the possibility of mild to severe adverse plant sensitisations. Being one of the poorest provinces in South Africa, the majority of specialist care, including dermatology in the Eastern Cape is only available in the major hospitals. Many health care centres are run by clinical officers or nurses, rather than physicians, who act as the primary care workers but have very limited training in diagnosing dermatologic conditions (Hay and Marks, 2004). Recently, the number of allergic patients in the world is increasing (BenShoshan et al., 2012). However, because of the relatively little data available in the scientific literature with regard to the adverse effects of plants in the Eastern Cape, the aim of this study therefore, was to document the plants responsible for allergic contact dermatitis (ACD) in the Eastern Cape, along with their respective allergens and to describe the clinical presentations observed in plant-induced ACD. A comprehensive inventory of allergenic plants is important for risk avoidance and diagnosis of allergic symptoms. In addition, a basic understanding of plant-induced allergic contact dermatitis and the common plants that cause each type can enable vulnerable individuals to discover the source of their dermatitis and thus prevent re-exposure. 2. Materials and methods 2.1. Description of the study area This study was carried out in the Amathole District (Fig. 1) of the Eastern Cape Province, South Africa. The Eastern Cape Province is one of the 9 provinces of South Africa and it falls within the latitudes
33
30°00′ to 34°15′S and longitudes 22°45′ to 30°15′E (Grierson and Afolayan, 1999). It is bounded by the sea in the East and the drier Karroo (semi-desert vegetation) in the west. The Amathole District Municipality is situated within the Eastern Cape Province, between Port Alfred and Port St John, and includes the city of East London. The climate is highly varied; the west is dry with sparse rain during winter or summer, with frosty winters and hot summers. Mean maximum temperature in January has been recorded as 26 °C and mean minimum as 10 °C in July. The main tribes of the area are Xhosa-speaking peoples who are divided into several tribes with related but distinct heritages. 2.2. Survey of plants that cause allergic contact dermatitis (ACD) The study was carried out by interviewing 161 respondents in 12 locations (Tyahli, Ngwenya, Dyamala, Gxwedera, Roxeni, Mhehelo, Sheshegu, Alice, Mavuso, Chwaru, Gaga and Fort Cox) in the Amathole District of the Eastern Cape. High poverty levels, lack of modern health facilities and the extensive use of medicinal plants are characteristic of the selected locations. Study participants were selected by convenient sampling with particular focus on local people who regularly interact with plants or plant products such as food handlers, caterers, cooks, chefs, gardeners, farmers, agricultural workers, florists, herbalists and nursery workers. The survey was conducted from April to June 2014, through interviews and discussions which were conducted in Xhosa — the local language of the informants and were facilitated by a local field assistant who is fluent in both Xhosa and English. The interviews included questions that targeted the local names of plants that cause allergies when they come in direct contact with
Fig. 1. Map of Amathole District Municipality. Source: Urban-Econ, Eastern Cape, 2011.
34
Family Scientific name Local name
Habit
Clinical presentation
Frequency of citation
Harm value
Principal use
Allergen
Reference
Amaryllidaceae Allium sativum L. Ivimbampunzi (garlic) Anacardiaceae Smodingium argutum E.Mey. ex Sond Umtomvane Anacardiaceae Mangifera indica L. Mango Anacardiaceae Anacardium occidentale L. Cashew nut tree Apiaceae Daucus carota L. Carrot Asteraceae Lactuca sativa L. Lettuce Asteraceae Artemisia afra Jacq. ex Willd. Umhlonyana Asteraceae Arctotheca calendula (L.) Levyns Isiqwashumbe (Cape dandelion) Asteraceae Erigeron bonariensis L. Asthmaweed Asteraceae Tagetes minuta L. Umva womfana Asteraceae Taraxacum campylodes G.E.Haglund Unomcwetshwana
Herb
Finger tip dermatitis
25
15.5
Food
Diallyl disulfide
Rozas-Muñoz et al. (2012)
Shrub
Rash is very oedematous
3
1.8
Weed
Heptadecyl catechols
Rozas-Muñoz et al. (2012)
Tree
Vesicles and generalised eruptions mostly limited to the angles of the mouth
33
20.4
Food
Urushiol
Wiwanitkit (2008)
Tree
Generalised eruptions and rashes
14
8.6
Food
Urushiol
Rozas-Muñoz et al. (2012)
Herb
Finger tip dermatitis
10
6.2
Food
Falcarinol
Rozas-Muñoz et al. (2012)
Herb
Sub-acute eczematous lesions of the face and neck
4
2.4
Food
Sesquiterpene lactone (SQL), lactucin and lactucopicrin
Rozas-Muñoz et al. (2012)
Shrub
Eczematous lesions of the exposed areas of the upper limbs
4
2.4
Medicinal
SQL
Rozas-Muñoz et al. (2012)
Herb
Eczematous lesions of the exposed areas of the upper limbs
3
1.8
Weed
SQL
Rozas-Muñoz et al. (2012)
Herb
Atopic eczema-like eruptions
2
1.2
Weed
SQL
Rozas-Muñoz et al. (2012)
Herb
Eczematous lesions of the exposed areas of the upper limbs
5
3.1
Food
Thiophenes, 5-(3-buten-1-ynyl)-2,2′-bithiophene, alpha-terthienyl and hydroxytremetone
Hausen and Helmke (1995)
Herb
Eczematous lesions of the exposed areas of the upper limbs
6
3.7
Weed
SQL, taraxanic acid
Jack et al. (2013)
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
Table 1 Plants responsible for causing allergic contact dermatitis.
Herb
Eczematous lesions of the exposed areas of the upper limbs
5
3.1
Medicinal
SQL, nobilin
Paulsen (2002)
Herb
Hand dermatitis
9
5.5
Food
Isothiocyanate
Rozas-Muñoz et al. (2012)
Herb
Hand dermatitis
8
4.9
Food
Isothiocyanate
Rozas-Muñoz et al. (2012)
Herb
Fingertip dermatitis, skin swelling
5
3.1
Food
Falcarinol
Rozas-Muñoz et al. (2012)
Shrub
Eczematous lesions of the exposed areas of the upper limbs
5
3.1
Ornamental
Phytosterol, 24-ethylcholestan-5-en-3-ol
Akoto et al. (2008)
Tree
Pain, erythema, severe conjunctival irritation
15
9.3
Food
Isothiocyanates
Rozas-Muñoz et al. (2012)
Tree
Blistering, erythema and itching
14
8.6
Commercial
Prohevein
Rozas-Muñoz et al. (2012)
Herb
Hand dermatitis
10
6.2
Food
ND
Tree
Hand dermatitis
18
11.1
Food
Geraniol, citral and D-limonene
Rozas-Muñoz et al. (2012)
Tree
Hand dermatitis
19
11.8
Food
Geraniol, citral and D-limonene
Rozas-Muñoz et al. (2012)
Herb
Itching, urticaria, and skin rash
26
16.1
Food
1,3-Beta-glucanase
Schmidt et al. (2002)
Herb
Urticaria, eczema, atopic dermatitis and itchy skin
25
15.5
Food
Patatin
Schmidt et al. (2002)
Herb
Localised itching, irritation, stinging or a rash
14
8.6
Food
Patatin
Schmidt et al. (2002)
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
Asteraceae Chamaemelum nobile (L.) All. Sweet chamomile Brassicaceae Brassica oleracea L. Cabbage Brassicaceae Brassica oleracea L. v botrytis Cauliflower Brassicaceae Apium graveolens L. Celery Capparaceae Capparis tomentosa Lam. Imfihlo Caricaceae Carica papaya L. Pawpaw Euphorbiaceae Hevea brasiliensis (Willd. ex A.Juss.) Müll.Arg. Rubber tree Musaceae Musa paradisiaca L. Banana Rutaceae Citrus limon (L.) Osbeck Lemon Rutaceae Citrus sinensis (L.) Osbeck Orange Solanaceae Capsicum annuum L. Itshilisi Solanaceae Solanum tuberosum L. Potato Solanaceae Solanum lycopersicum L. Tomato
35
36
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
the skin. The symptomatology (rash, erythema, itchy skin, swelling, lesions, oozing, scarring of the skin, etc.) of various skin allergies was described to the informants so as to enable them to state the appropriate culprit plant species. The plant parts implicated and the life forms of the reported plants were also recorded. The local names of the plants were cross-checked in different locations either by showing the plant specimen or telling the local names of plants to other informants in order to verify the authenticity of claims (Abbasi et al., 2010). 2.3. Identification and collection of allergenic plants Collection of plants reported as causing ACD was assisted by the informants in order to ensure that the correct plants have been collected. The fresh plant materials were pressed and mounted on herbarium sheets and were later transported to the University of Fort Hare's herbarium where identification of the collected plant specimens was done in the Department of Botany with the help of floristic works of South Africa (Dold and Cocks, 2000) and the Plant List (www. theplantlist.org/). Voucher specimens were deposited in the Griffin Herbarium of the University of Fort Hare. 2.4. Data analysis The harm-value, modified from Phillips et al. (1994), that was used as a quantitative index that weighs the relative local significance of a plant species as a causative agent of allergic contact dermatitis was calculated as follows: HV ¼ ΣU=n where: HV = harm-value of a species; U = number of citations per species; and n = number of informants. 2.5. Intellectual property agreement The survey was carried out with the full consent of all participants, with further verbal agreement and understanding that this research shall not be used for commercial purposes, but shall serve as enlightenment and as a means of preservation of the indigenous knowledge as regards plant-induced ACD in the Eastern Cape, South Africa. Ethical approval for the study was granted by the Ethics Committee of the University of Fort Hare. 3. Results and discussion 3.1. Socio-demographic information Out of 161 informants, 62 (39%) were males and 99 (61%) were females; aged between 19 and 76 years with a mean age of 35.1 ± 14.2. The higher proportion of female respondents as compared to men was probably due to the fact that occupations that are more vulnerable to plant-induced ACD such as food handlers, professional cooks and chefs are mostly dominated by females. 3.2. Diversity of plants that cause allergic contact dermatitis (ACD) Results of the present investigation are presented in Table 1. In the current study, 24 plant species distributed in 11 families were reported as causative agents of ACD. The most representative families were Asteraceae (7 species), Solanaceae, Anarcadiaceae and Rutaceae (3 species each) (Fig. 2). Herbs constituted 62.50%, trees 25.0% and shrubs 12.50%. The species with the highest frequency of citations were Mangifera indica (33 citations), Capsicum annuum (26 citations) and Allium sativum and Solanum tuberosum (25 citations each).
3.2.1. Asteraceae (Compositae) species causing allergic contact dermatitis The Asteraceae is the second largest family of flowering plants in the world and over 200 species of this family are important causes of contact dermatitis worldwide (Paulsen, 2002). In this study, the Asteraceae was probably the most important allergenic plant family mentioned, represented by the highest number of species (Fig. 2); including commonly used medicinal plants such as Artemisia afra, vegetables such as Lactuca sativa and weeds such as Conyza bonariensis and Arctotheca calendula (Table 1). The species with the highest number of citations for ACD were Tagetes minuta (Mexican marigold) and Chamaemelum nobile (Sweet chamomile) with 5 citations each, followed by Taraxacum campylodes with 4 citations. Sub-acute eczematous lesions of the face, neck, and the exposed areas of the upper limbs are characteristic of Asteraceae allergies. T. minuta, known locally as Umva womfana, is a common weed in South Eastern Africa and has a vesicant primary irritant effect on intact skin and can cause severe and prolonged allergic contact dermatitis, with cross-sensitisation to other Compositae plants. As early as 1895, allergy to T. minuta was reported. Several species of Tagetes are strongly aromatic and potentially irritant. There are reports of occupational dermatitis to Tagetes patula in an aromatherapist (Bilsland and Strong, 1990). Sweet chamomile (C. nobile) has been planted in lawns since the early Elizabethan times. The dried flowers are used to make chamomile tea and chamomile oil is used for the prevention and treatment of nappy rash and as a nipple cream. On the other hand, chamomile has been reported to cause allergic dermatitis on a number of occasions. In a six year study in Germany, 67 patients were found to be allergic to chamomile and in another study of massage in children with atopic eczema, a number of the children went on to develop worsening of their atopic eczema due to allergy to the essential oils, including chamomile (Anderson et al., 2000). The allergens in chamomile include nobilin (Sweet chamomile) and desacetylmatricarin (German chamomile). Both are sesquiterpene lactones. Sesquiterpene lactones (SQLs) are 15-carbon molecules made up of a sesquiterpene linked to a lactone ring (Paulsen, 2002) and they are the most important allergens in the Asteraceae family, present in the oleoresin fraction of leaf, stem, flower and possibly in the pollen. The allergenicity is increased by the presence of an α-methylene group attached to the lactone ring.
3.2.2. Solanaceae species causing allergic contact dermatitis Capsicum annuum (pepper), S. tuberosum (potato) and Solanum lycopersicum (tomato) were the Solanaceae species that were associated to ACD dermatitis with citations of 26, 25 and 14 respectively (Table 1). C. annuum (Sweet, Green or Bell pepper) and Capsicum frutescens (Cayenne or Chili pepper) are 2 peppers of the Solanacea family which are used mainly as vegetables. Urticaria, skin rash and itches were the allergies associated to C. annuum while allergic reactions characterised by urticaria, eczema, atopic dermatitis and itchy skin triggered by exposure to raw, cut potato were reported (Table 1). Exposures to allergen occur during direct contact with potato peelings at home or in food processing plants or after inhalation of potato pollen by farm workers. Studies on the allergens in potato have mainly concentrated on one protein called patatin (Schmidt et al., 2002). This allergen can cause reactions such as eczema and has been implicated in atopic dermatitis. Patatin is sensitive to heat, hence, cooked potatoes no longer have the potential to cause allergic reactions; therefore, potatoes are viewed as ‘safe’ for individuals suffering from food allergies and form the staple food in many countries. Allergic contact dermatitis to tomato was reported as localised and mild itching, irritation, or rash symptoms in the mouth triggered by eating raw tomatoes. The common observation that some people exhibit allergic symptoms to raw tomato is important to the food industry considering the increasing consumption of raw tomatoes in salads worldwide. Ten out of 17 patients (25%) reported allergic reactions to cooked tomatoes; in immunoblotting tests, their sera
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
7
3.2.5. Amaryllidaceae species causing allergic contact dermatitis Amaryllidaceae family members can be recognised easily by their characteristic garlic smell as well as their soft, fleshy leaves. The genus Allium is the most important genus in dermatology and includes many important vegetables such as garlic and onion. Garlic is the only species in the Amaryllidaceae family that was reported for allergic contact dermatitis. All parts of the plant, when damaged, release the potentially irritating and allergenic sap. Diallyl disulfide, allicin, and allyl propyl disulfide have been identified as the principal low molecular weight allergens.
6
No of species
37
5 4 3 2 1 0
Plant families Fig. 2. Plant families implicated in allergic contact dermatitis.
reacted only to lipid transfer protein (LTP) (Pravettoni et al., 2009). In fresh tomato, different LTP isoforms are present and allergenic. 3.2.3. Anarcadiaceae species causing allergic contact dermatitis In the current study, the causes of allergic phytodermatitis in the Anacardeaceae family include M. indica (mango fruit tree), Anacardium occidentale (cashew nut tree) and Smodingium argutum (South African poison ivy) (Table 1). Mango was the most cited (33 citations) cause of ACD in the study area and dermatitis occurs when the sap of the skin, bruised leaf, or stem of the fruit touches the skin. Dermatitis may present as vesicles, dermal lesions or generalised eruptions mostly limited to the angles of the mouth, although the hands may carry the allergens to the eyes and neck. The responsible allergens are urushiol and other sensitising substances include cardol, limonene and Bpinene (Oka et al., 2004). These allergens are found in the stems, leaves, and peel, but not in fruit juice, hence the juice may be drunk by sensitised persons (Wiwanitkit, 2008). Delayed hypersensitivity to mango is CD-4 cells mediated. Allergens in mango sap sensitise CD-4 cells which on repeated exposure migrate towards the epidermis where they release cytokine-damaging keratinocytes, leading to epidermal spongiosis which reaches a peak in 24–72 h, and then slowly subsides. This accounts for the later onset of symptoms in allergic individuals. The African poison ivy (S. argutum) is a Southern African shrub which is monotypic in the genus Smodingium, and was discovered in Pondoland by J. F. Drège during an 1832 expedition with the zoologist Andrew Smith. It is found only in South Africa and there is no other species in the genus. The plant has properties comparable to the American poison ivy, as its sap contains heptadecyl catechols that are toxic to the skin, its immuno-chemical reaction is common in other toxic anacardiaceous species and the rash is very oedematous (Findlay, 1963). The middle layer of cashew nut is filled with a brownish oil rich in cardol and anacardic acid, chemically similar to urushiol. These catechols are destroyed when the nut is properly roasted and processed, but harvesters can develop allergic phytodermatitis from exposure to the oil. 3.2.4. Citrus species causing allergic contact dermatitis Besides its use in the food industry, Citrus spp are used for aromatic oils for perfumery and in the manufacture of soaps and cosmetics. The species associated to ACD in the study area are Citrus sinensis (sweet orange) and Citrus limon (lemon) with 19 and 18 citations respectively (Table 1). Hand dermatitis was reported especially by food handlers. The potential sensitisers in Citrus spp include geraniol, citral and the hydroperoxide derivative of D-limonene, which are usually included in fragrances. The mechanism of sensitisation is currently an object of research.
3.2.6. Capparaceae species causing allergic contact dermatitis The Capparaceae family is regarded as the tropical relative of the mustard family, which comprises some 650 species of small trees and shrubs in 30 genera (Rozas-Muñoz et al., 2012). The species of this family associated to ACD in the study area is Capparis spinosa, or caper bush, a shrub with greyish oval leaves and showy white-pink flowers with several prominent stamens. C. spinosa contains thioglucosides, which are broken down enzymatically, in the presence of water, to isothiocyanates, potent irritants, which appear to be also the most important allergens (Dannaker and White, 1987). Contact dermatitis from this plant was reported as eczematous eruption of the exposed areas of the upper limbs. 3.2.7. Apiaceae species causing allergic contact dermatitis Carrot (Daucus carota) is a root vegetable of usually orange colour which was previously grown for its aromatic leaves and seeds but it is now cultivated mainly for food. Allergic contact dermatitis induced by carrot was reported as hand or finger-tip dermatitis (Table 1). The responsible allergen has been identified as falcarinol, an allergen also present in celery (Apium graveolens L.) (Murdoch and Dempster, 2000). Occupational allergic contact dermatitis induced by carrot is well recognised, particularly affecting employees working in canning factories (Rozas-Muñoz et al., 2012). 3.3. Occupational exposure to plant-induced allergic contact dermatitis Out of the 24 plant species that were mentioned in the survey for causing ACD, 67% are principally used as food (Fig. 3). This finding implies that workers within the food industries (such as bakers, caterers, cooks, chefs, etc.) have a higher-than-average risk of contacting plant-induced ACD. Occupational dermatitis has been frequently reported in the literature. In garlic for example, the typical occupational gesture of cutting the bulb, which is held between the thumb and the first/second finger of the non-dominant hand leads to the characteristic distribution of hyperkeratotic eczema on the tips of the fingers (Ekeowa-Anderson et al., 2007). Allergy occurring soon after contact with rubber latex was reported as blisters, scaling and erythema. Approximately 10% of health personnel who are occupationally exposed to rubber gloves and other rubber
Ornamental 4% Medicinal 8%
Commercial 4% Weed 17%
Food 67%
Fig. 3. Principal uses of plants reported for causing irritant contact dermatitis.
38
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
articles have a particularly high incidence of allergy to natural rubber latex. Latex is the milky sap of Hevea brasiliensis tree, which is processed to manufacture multiple products, including gloves, condoms and balloons. Latex allergy has been recognised as a very important health problem, due to an increase in frequency, and to its ability to induce severe reactions. The protein content of natural rubber triggers a Type-4 delayed immunological reaction which is extremely itchy and uncomfortable. Although the true prevalence of occupational allergic contact dermatitis in South Africa is not known, a high burden of occupational skin disease will definitely translate into large costs in terms of days lost from work and adjustments necessary in the workplace. Hence, early recognition of allergic contact dermatitis may lead to improved outcomes to both employees and employers. Therefore, health care practitioners need to be aware of possible occupational causes for all cases of ACD.
workplace. Hence, early recognition of allergic contact dermatitis may lead to improved outcomes to both employees and employers. Therefore, health care practitioners need to be aware of possible occupational causes for all cases of ACD. Competing interest The authors declare that there is no conflict of interests regarding the publication of this paper. Authors' contributions WOM designed the study and took part in data collection and analysis, DSG took part in data collection and writing of the manuscript, and AJA took part in writing and editing of the manuscript.
3.4. Cross-reactions to different plant allergens Acknowledgements Allergy to a particular plant rarely presents as an isolated disorder, due to cross-reactivity with similar allergens in other plants. Crossreactivity or cross-sensitisation is a term used to describe a phenomenon where the allergen to which a person is sensitive is present in different plants, resulting in that person being allergic to those different plants. Our immune systems recognise particular antigen structures as foreign without regard to the origin of these molecules. Close structural similarities between any two allergens from divergent sources can produce similar allergic reactions in sensitive individuals. Two patterns of associated allergies were identified among the plants implicated for ACD in the current study: mango plant allergy with celery, carrot, tomato, papaya and banana and rubber latex allergy with banana, pepper and potato, a condition known as the latex-fruit syndrome. Allergens responsible for this syndrome seem to be a group of shared plant proteins, to which patients react. This cross reactivity is attributed to the fact that multiple antigens can bind to an immunoglobulin E (IgE) antibody at corresponding sites resulting to an immune response. For example, several types of proteins have been identified as being involved in the latex-fruit syndrome such as class I chitinases (Rozynek et al., 2006) from banana containing an N-terminal heveinlike domain which cross-reacts with hevein (Hev b6.02), a major IgE allergen for patients allergic to natural rubber latex. Other important natural rubber latex-allergens are Hev b 2 (which shows crossreactivity with proteins of bell pepper) and Hev b 7, a patatin-like protein (cross-reacts with its homologous protein in potato). These proteins seem to be inactivated by heating, which could explain why some plant foods that contain these allergens are not associated with this syndrome when consumed after cooking. 3.5. Conclusion The current study was undertaken to investigate and document plants responsible for allergic contact dermatitis (ACD) in the Eastern Cape. Twenty four plant species distributed in 11 families were reported as causative agents of ACD. The most representative families were Asteraceae, Solanaceae, Anarcadiaceae and Rutaceae. Herbs constituted 62.50%, trees 25.0% and shrubs 12.50%. The Asteraceae was the most important allergenic plant family, represented by the highest number of species. Mango (Mangifera indica) was the most cited cause of ACD in the study area. Two patterns of associated allergies were identified among the plants implicated for ACD in the current study: mango plant allergy with celery, carrot, tomato, papaya and banana and rubber latex allergy with banana, pepper and potato. Out of the 24 plant species that were mentioned in the survey for causing ACD, 67% are principally used as food. Although the true prevalence of occupational allergic contact dermatitis in South Africa is not known, a high burden of occupational skin disease will definitely translate into large costs in terms of days lost from work and adjustments necessary in the
The authors greatly appreciate the National Research Foundation (NRF) (grant no. T304) and Govan Mbeki Research and Development Centre (GMRDC) of the University of Fort Hare, South Africa (grant no. C295) for financing this study. References Abbasi, A.M., Khan, M.A., Ahmad, M., Zafar, M., Jahan, S., Sultana, S., 2010. Ethnopharmacological application of medicinal plants to cure skin diseases and in folk cosmetics among the tribal communities of North-West Frontier Province. Pakistan Journal of Ethnopharmacology 128, 322–335. Akoto, O., Oppong, I.V., Addae-Mensah, I., Waibel, R., Achenbach, H., 2008. Isolation and characterization of dipeptide derivative and phytosterol from Capparis tomentosa Lam. Scientifc Research and Essays 3, 355–358. Anderson, C., Lis-Balchin, M., Kirk-Smith, M., 2000. Evaluation of massage with essential oils on childhood atopic eczema. Phytotherapy Research 14, 452–456. Ben-Shoshan, M., Turnbull, E., Clarke, A., 2012. Food allergy: temporal trends and determinants. Current Allergy and Asthma Reports 12, 346–372. Bhat, R.B., Jacobs, T.V., 1985. Traditional herbal medicine in Transkei. Journal of Ethnopharmacology 48, 7–12. Bilsland, D., Strong, A., 1990. Allergic contact dermatitis from the essential oil of French marigold (Tagetes patula) in an aromatherapist. Contact Dermatitis 23, 55–56. Dannaker, C.J., White, I.R., 1987. Cutaneous allergy to mustard in a salad maker. Contact Dermatitis 16, 212–214. Dold, A.P., Cocks, M.L., 2000. Indigenous plant use of the amaXhosa people on the Eastern border of the Great Fish River Reserve, Eastern Cape. Annals of the Eastern Cape Museum 1, 26–53. Ekeowa-Anderson, A.L., Shergil, B., Goldsmith, P., 2007. Allergic contact cheilitis to garlic. Contact Dermatitis 56, 174–175. Findlay, G.H., 1963. Dermatitis of ‘poison ivy’ type from an indigenous South African Plant —Smodingium argutum E. Mey. (Anacardiaceae). South African Medical Journal 37, 883–888. Grierson, D.S., Afolayan, A.J., 1999. Antibacterial activity of some indigenous plants used for the treatment of wounds in the Eastern Cape, South Africa. Journal of Ethnopharmacology 66, 103–106. Hausen, B.M., Helmke, B., 1995. Butenylbithiophene, alpha-terthienyl and hydroxytremetone as contact allergens in cultivars of marigold (Tagetes sp.). Contact Dermatitis 33, 33–37. Hay, R., Marks, R., 2004. The International Foundation for Dermatology: an exemplar of the increasingly diverse activities of the International League of Dermatological Societies. British Journal of Dermatology 150, 747–749. Jack, A.R., Norris, P.L., Storrs, S.J., 2013. Allergic contact dermatitis to plant extracts in cosmetics. Seminars in Cutaneous Medicine and Surgery 32, 140–146. Modi, G.M., Doherty, C.B., Katta, R., Orengo, I.F., 2009. Irritant contact dermatitis from plants. Dermatitis 20, 63–78. Murdoch, S.R., Dempster, J., 2000. Allergic contact dermatitis from carrot. Contact Dermatitis 42, 236. Oka, K., Saito, F., Yasuhara, T., Sugimoto, A., 2004. A study of cross reactions between mango contact allergens and urushiol. Contact Dermatitis 5, 292–296. Paulsen, E., 2002. Contact sensitization from Compositae-containing herbal remedies and cosmetics. Contact Dermatitis 47, 189–198. Phillips, O., Gentry, A.H., Reynel, C., Wilkin, P., Gálvez- Durand, C., 1994. Quantitative ethnobotany and Amazonian conservation. Conservation Biology 8, 225–248. Phillipson, P.B., 1987. A checklist of vascular plants of the Amatole Mountains, Eastern Cape Province: Ciskei. Bothalia 17237–17256. Pravettoni, V., Primavesi, L., Farioli, L., Brenna, O.V., Pompei, C., Conti, A., Scibilia, J., Piantanida, M., Mascheri, A., Pastorello, E.A., 2009. Tomato allergy: detection of IgEbinding lipid transfer proteins in tomato derivatives and in fresh tomato peel, pulp, and seeds. Journal of Agriculture and Food Chemistry 57, 10749–10754.
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39 Rozas-Muñoz, E., Lepoittevin, J.P., Pujol, R.M., Giménez-Arnau, A., 2012. Allergic contact dermatitis to plants: understanding the chemistry will help our diagnostic approach. Actas Dermosifiliograficas 103, 456–477. Rozynek, P., Rihs, H.P., Gaspar, A., Brüning, T., Raulf-Heimsoth, M., 2006. The new Hev b 7.02 iso-allergen from Hevea brasiliensis is an important allergen for health care workers and spina bifida patients. Allergy 61, 508–509. Saint-Mezard, P., Rosieres, A., krasteva, M., Berard, F., Dubois, B., kaiserlian, D., Nicolas, J., 2004. Allergic contact dermatitis. European Journal of Dermatology 14, 284–295.
39
Sasseville, D., 1999. Phytodermatitis. Journal of Cutaneous Medicine and Surgery 3, 263–279. Schmidt, M.H., Raulf-Heimsoth, M., Posch, A., 2002. Evaluation of patatin as a major crossreactive allergen in latex-induced potato allergy. Allergy 146, 131–135. van Ketel, W.G., 1975. A cauliflower allergy. Contact Dermatitis 1, 324–325. Wiwanitkit, V., 2008. Mango dermatitis. Indian Journal of Dermatology 53, 158.
Contents lists available at ScienceDirect
South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb
A survey of plants responsible for causing allergic contact dermatitis in the Amathole District, Eastern Cape, South Africa Wilfred Mbeng Otang 1, Donald Scott Grierson 2, Anthony Jide Afolayan ⁎ MPED Research Centre, Department of Botany, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa
a r t i c l e
i n f o
Article history: Received 6 November 2014 Received in revised form 8 December 2014 Accepted 23 December 2014 Available online 14 January 2015 Edited by J Van Staden Keywords: Survey Allergic contact dermatitis Eastern Cape, South Africa
a b s t r a c t Background: An inventory of allergenic plants can enable vulnerable individuals to discover the source of their dermatitis and thus prevent re-exposure. However, because of the relatively little data available in the scientific literature with regard to the adverse effects of plant, the aim of this study was to document the plants responsible for allergic contact dermatitis (ACD) in the Eastern Cape. Interview questions targeted the local names of plants that cause allergies when in direct contact with the skin. Results: Twenty four plant species in 11 families were reported as causative agents of ACD. The Asteraceae was probably the most important allergenic plant family, represented by commonly used medicinal plants such as Artemisia afra, vegetables such as Lactuca sativa and weeds such as Conyza bonariensis. Sub-acute eczematous lesions of the face and the exposed areas of the upper limbs were characteristic of Asteraceae allergies. Out of the 24 plants mentioned for causing ACD, 67% are principally used as food. Conclusions: A high burden of occupational skin disease in the food industry will definitely translate into large costs in terms of days lost from work and adjustments necessary in the workplace. Therefore, health care practitioners need to be aware of possible occupational causes for all cases of ACD. © 2015 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction The skin is the largest organ of the human body. As the outermost barrier of the human body, it is the first to encounter chemical and physical factors from the environment and therefore prone to many health problems. Numerous occupations are associated with the risk of developing reactions to plants. These include food handlers, caterers, market gardeners, farmers, agricultural workers, florists, nursery workers, landscapers, forestry workers and loggers. It is estimated that 50% of agricultural occupational skin disease is due to plants, trees and natural vegetation (Modi et al., 2009). Plants can harm the skin in numerous ways: irritant contact dermatitis due to mechanical injury or by irritant chemicals in the plant sap, phytophotodermatitis resulting from skin contamination by plants containing furocoumarins following subsequent exposure to UV light and immediate (type I) or delayed hypersensitivity contact reactions mediated by the immune system in individuals sensitised to plants or plant products e.g. peanut allergy and poison ivy poisoning (van Ketel, 1975). Dermatitis and eczema are used synonymously to denote a polymorphous pattern of skin inflammation characterised at least in its acute phase by erythema,
⁎ Corresponding author. Tel.: +27 406022323; fax: +27 86 628 2295. E-mail addresses: [email protected] (W.M. Otang), [email protected] (D.S. Grierson), [email protected] (A.J. Afolayan). 1 Tel.: +27 33257274; fax: +27 866282409. 2 Tel.: +27 406022321; fax: +27 866282409.
http://dx.doi.org/10.1016/j.sajb.2014.12.006 0254-6299/© 2015 SAAB. Published by Elsevier B.V. All rights reserved.
vesiculation and pruritus (Saint-Mezard et al., 2004) while an allergy is an immune reaction causing local or systemic acute inflammation in susceptible individuals after repeated exposure to certain antigens. Approximately one third of people will suffer from an allergy at some time in their lives and 15–20% of children suffer from atopic eczema (Ben-Shoshan et al., 2012). Allergic contact dermatitis (ACD) is a T-cell-mediated inflammatory reaction of the skin that occurs in sensitised individuals (Modi et al., 2009). ACD requires the activation of antigen-specific acquired immunity leading to the development of effector T cells which mediate the inflammation. It is characterised by redness, papules and vesicles, followed by scaling and dry skin. Unlike irritant dermatitis, allergic contact dermatitis requires previous sensitisation to the allergen and a sensitised immune system; hence, not everyone will develop an allergy to a culprit compound (Sasseville, 1999). The Eastern Cape Province of South Africa is particularly known for its richness in plant species (Phillipson, 1987). The Xhosas, who are the major inhabitants of this province had no interaction with the Western world for many years, hence, they relied mainly on traditional knowledge of medicinal plants for the treatment of various diseases and ailments. The daily activities of the Xhosa people are centred mainly on agriculture: cattle rearing and the production of crops and vegetables in small fields along the rivers and in home gardens (Bhat and Jacobs, 1985). In addition to agriculture the gathering of wild fruits and other edible plant parts, the collection of honey and the hunting of wildlife also contribute to their livelihood. This high interaction with plants on
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
a daily basis may theoretically result in the possibility of mild to severe adverse plant sensitisations. Being one of the poorest provinces in South Africa, the majority of specialist care, including dermatology in the Eastern Cape is only available in the major hospitals. Many health care centres are run by clinical officers or nurses, rather than physicians, who act as the primary care workers but have very limited training in diagnosing dermatologic conditions (Hay and Marks, 2004). Recently, the number of allergic patients in the world is increasing (BenShoshan et al., 2012). However, because of the relatively little data available in the scientific literature with regard to the adverse effects of plants in the Eastern Cape, the aim of this study therefore, was to document the plants responsible for allergic contact dermatitis (ACD) in the Eastern Cape, along with their respective allergens and to describe the clinical presentations observed in plant-induced ACD. A comprehensive inventory of allergenic plants is important for risk avoidance and diagnosis of allergic symptoms. In addition, a basic understanding of plant-induced allergic contact dermatitis and the common plants that cause each type can enable vulnerable individuals to discover the source of their dermatitis and thus prevent re-exposure. 2. Materials and methods 2.1. Description of the study area This study was carried out in the Amathole District (Fig. 1) of the Eastern Cape Province, South Africa. The Eastern Cape Province is one of the 9 provinces of South Africa and it falls within the latitudes
33
30°00′ to 34°15′S and longitudes 22°45′ to 30°15′E (Grierson and Afolayan, 1999). It is bounded by the sea in the East and the drier Karroo (semi-desert vegetation) in the west. The Amathole District Municipality is situated within the Eastern Cape Province, between Port Alfred and Port St John, and includes the city of East London. The climate is highly varied; the west is dry with sparse rain during winter or summer, with frosty winters and hot summers. Mean maximum temperature in January has been recorded as 26 °C and mean minimum as 10 °C in July. The main tribes of the area are Xhosa-speaking peoples who are divided into several tribes with related but distinct heritages. 2.2. Survey of plants that cause allergic contact dermatitis (ACD) The study was carried out by interviewing 161 respondents in 12 locations (Tyahli, Ngwenya, Dyamala, Gxwedera, Roxeni, Mhehelo, Sheshegu, Alice, Mavuso, Chwaru, Gaga and Fort Cox) in the Amathole District of the Eastern Cape. High poverty levels, lack of modern health facilities and the extensive use of medicinal plants are characteristic of the selected locations. Study participants were selected by convenient sampling with particular focus on local people who regularly interact with plants or plant products such as food handlers, caterers, cooks, chefs, gardeners, farmers, agricultural workers, florists, herbalists and nursery workers. The survey was conducted from April to June 2014, through interviews and discussions which were conducted in Xhosa — the local language of the informants and were facilitated by a local field assistant who is fluent in both Xhosa and English. The interviews included questions that targeted the local names of plants that cause allergies when they come in direct contact with
Fig. 1. Map of Amathole District Municipality. Source: Urban-Econ, Eastern Cape, 2011.
34
Family Scientific name Local name
Habit
Clinical presentation
Frequency of citation
Harm value
Principal use
Allergen
Reference
Amaryllidaceae Allium sativum L. Ivimbampunzi (garlic) Anacardiaceae Smodingium argutum E.Mey. ex Sond Umtomvane Anacardiaceae Mangifera indica L. Mango Anacardiaceae Anacardium occidentale L. Cashew nut tree Apiaceae Daucus carota L. Carrot Asteraceae Lactuca sativa L. Lettuce Asteraceae Artemisia afra Jacq. ex Willd. Umhlonyana Asteraceae Arctotheca calendula (L.) Levyns Isiqwashumbe (Cape dandelion) Asteraceae Erigeron bonariensis L. Asthmaweed Asteraceae Tagetes minuta L. Umva womfana Asteraceae Taraxacum campylodes G.E.Haglund Unomcwetshwana
Herb
Finger tip dermatitis
25
15.5
Food
Diallyl disulfide
Rozas-Muñoz et al. (2012)
Shrub
Rash is very oedematous
3
1.8
Weed
Heptadecyl catechols
Rozas-Muñoz et al. (2012)
Tree
Vesicles and generalised eruptions mostly limited to the angles of the mouth
33
20.4
Food
Urushiol
Wiwanitkit (2008)
Tree
Generalised eruptions and rashes
14
8.6
Food
Urushiol
Rozas-Muñoz et al. (2012)
Herb
Finger tip dermatitis
10
6.2
Food
Falcarinol
Rozas-Muñoz et al. (2012)
Herb
Sub-acute eczematous lesions of the face and neck
4
2.4
Food
Sesquiterpene lactone (SQL), lactucin and lactucopicrin
Rozas-Muñoz et al. (2012)
Shrub
Eczematous lesions of the exposed areas of the upper limbs
4
2.4
Medicinal
SQL
Rozas-Muñoz et al. (2012)
Herb
Eczematous lesions of the exposed areas of the upper limbs
3
1.8
Weed
SQL
Rozas-Muñoz et al. (2012)
Herb
Atopic eczema-like eruptions
2
1.2
Weed
SQL
Rozas-Muñoz et al. (2012)
Herb
Eczematous lesions of the exposed areas of the upper limbs
5
3.1
Food
Thiophenes, 5-(3-buten-1-ynyl)-2,2′-bithiophene, alpha-terthienyl and hydroxytremetone
Hausen and Helmke (1995)
Herb
Eczematous lesions of the exposed areas of the upper limbs
6
3.7
Weed
SQL, taraxanic acid
Jack et al. (2013)
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
Table 1 Plants responsible for causing allergic contact dermatitis.
Herb
Eczematous lesions of the exposed areas of the upper limbs
5
3.1
Medicinal
SQL, nobilin
Paulsen (2002)
Herb
Hand dermatitis
9
5.5
Food
Isothiocyanate
Rozas-Muñoz et al. (2012)
Herb
Hand dermatitis
8
4.9
Food
Isothiocyanate
Rozas-Muñoz et al. (2012)
Herb
Fingertip dermatitis, skin swelling
5
3.1
Food
Falcarinol
Rozas-Muñoz et al. (2012)
Shrub
Eczematous lesions of the exposed areas of the upper limbs
5
3.1
Ornamental
Phytosterol, 24-ethylcholestan-5-en-3-ol
Akoto et al. (2008)
Tree
Pain, erythema, severe conjunctival irritation
15
9.3
Food
Isothiocyanates
Rozas-Muñoz et al. (2012)
Tree
Blistering, erythema and itching
14
8.6
Commercial
Prohevein
Rozas-Muñoz et al. (2012)
Herb
Hand dermatitis
10
6.2
Food
ND
Tree
Hand dermatitis
18
11.1
Food
Geraniol, citral and D-limonene
Rozas-Muñoz et al. (2012)
Tree
Hand dermatitis
19
11.8
Food
Geraniol, citral and D-limonene
Rozas-Muñoz et al. (2012)
Herb
Itching, urticaria, and skin rash
26
16.1
Food
1,3-Beta-glucanase
Schmidt et al. (2002)
Herb
Urticaria, eczema, atopic dermatitis and itchy skin
25
15.5
Food
Patatin
Schmidt et al. (2002)
Herb
Localised itching, irritation, stinging or a rash
14
8.6
Food
Patatin
Schmidt et al. (2002)
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
Asteraceae Chamaemelum nobile (L.) All. Sweet chamomile Brassicaceae Brassica oleracea L. Cabbage Brassicaceae Brassica oleracea L. v botrytis Cauliflower Brassicaceae Apium graveolens L. Celery Capparaceae Capparis tomentosa Lam. Imfihlo Caricaceae Carica papaya L. Pawpaw Euphorbiaceae Hevea brasiliensis (Willd. ex A.Juss.) Müll.Arg. Rubber tree Musaceae Musa paradisiaca L. Banana Rutaceae Citrus limon (L.) Osbeck Lemon Rutaceae Citrus sinensis (L.) Osbeck Orange Solanaceae Capsicum annuum L. Itshilisi Solanaceae Solanum tuberosum L. Potato Solanaceae Solanum lycopersicum L. Tomato
35
36
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
the skin. The symptomatology (rash, erythema, itchy skin, swelling, lesions, oozing, scarring of the skin, etc.) of various skin allergies was described to the informants so as to enable them to state the appropriate culprit plant species. The plant parts implicated and the life forms of the reported plants were also recorded. The local names of the plants were cross-checked in different locations either by showing the plant specimen or telling the local names of plants to other informants in order to verify the authenticity of claims (Abbasi et al., 2010). 2.3. Identification and collection of allergenic plants Collection of plants reported as causing ACD was assisted by the informants in order to ensure that the correct plants have been collected. The fresh plant materials were pressed and mounted on herbarium sheets and were later transported to the University of Fort Hare's herbarium where identification of the collected plant specimens was done in the Department of Botany with the help of floristic works of South Africa (Dold and Cocks, 2000) and the Plant List (www. theplantlist.org/). Voucher specimens were deposited in the Griffin Herbarium of the University of Fort Hare. 2.4. Data analysis The harm-value, modified from Phillips et al. (1994), that was used as a quantitative index that weighs the relative local significance of a plant species as a causative agent of allergic contact dermatitis was calculated as follows: HV ¼ ΣU=n where: HV = harm-value of a species; U = number of citations per species; and n = number of informants. 2.5. Intellectual property agreement The survey was carried out with the full consent of all participants, with further verbal agreement and understanding that this research shall not be used for commercial purposes, but shall serve as enlightenment and as a means of preservation of the indigenous knowledge as regards plant-induced ACD in the Eastern Cape, South Africa. Ethical approval for the study was granted by the Ethics Committee of the University of Fort Hare. 3. Results and discussion 3.1. Socio-demographic information Out of 161 informants, 62 (39%) were males and 99 (61%) were females; aged between 19 and 76 years with a mean age of 35.1 ± 14.2. The higher proportion of female respondents as compared to men was probably due to the fact that occupations that are more vulnerable to plant-induced ACD such as food handlers, professional cooks and chefs are mostly dominated by females. 3.2. Diversity of plants that cause allergic contact dermatitis (ACD) Results of the present investigation are presented in Table 1. In the current study, 24 plant species distributed in 11 families were reported as causative agents of ACD. The most representative families were Asteraceae (7 species), Solanaceae, Anarcadiaceae and Rutaceae (3 species each) (Fig. 2). Herbs constituted 62.50%, trees 25.0% and shrubs 12.50%. The species with the highest frequency of citations were Mangifera indica (33 citations), Capsicum annuum (26 citations) and Allium sativum and Solanum tuberosum (25 citations each).
3.2.1. Asteraceae (Compositae) species causing allergic contact dermatitis The Asteraceae is the second largest family of flowering plants in the world and over 200 species of this family are important causes of contact dermatitis worldwide (Paulsen, 2002). In this study, the Asteraceae was probably the most important allergenic plant family mentioned, represented by the highest number of species (Fig. 2); including commonly used medicinal plants such as Artemisia afra, vegetables such as Lactuca sativa and weeds such as Conyza bonariensis and Arctotheca calendula (Table 1). The species with the highest number of citations for ACD were Tagetes minuta (Mexican marigold) and Chamaemelum nobile (Sweet chamomile) with 5 citations each, followed by Taraxacum campylodes with 4 citations. Sub-acute eczematous lesions of the face, neck, and the exposed areas of the upper limbs are characteristic of Asteraceae allergies. T. minuta, known locally as Umva womfana, is a common weed in South Eastern Africa and has a vesicant primary irritant effect on intact skin and can cause severe and prolonged allergic contact dermatitis, with cross-sensitisation to other Compositae plants. As early as 1895, allergy to T. minuta was reported. Several species of Tagetes are strongly aromatic and potentially irritant. There are reports of occupational dermatitis to Tagetes patula in an aromatherapist (Bilsland and Strong, 1990). Sweet chamomile (C. nobile) has been planted in lawns since the early Elizabethan times. The dried flowers are used to make chamomile tea and chamomile oil is used for the prevention and treatment of nappy rash and as a nipple cream. On the other hand, chamomile has been reported to cause allergic dermatitis on a number of occasions. In a six year study in Germany, 67 patients were found to be allergic to chamomile and in another study of massage in children with atopic eczema, a number of the children went on to develop worsening of their atopic eczema due to allergy to the essential oils, including chamomile (Anderson et al., 2000). The allergens in chamomile include nobilin (Sweet chamomile) and desacetylmatricarin (German chamomile). Both are sesquiterpene lactones. Sesquiterpene lactones (SQLs) are 15-carbon molecules made up of a sesquiterpene linked to a lactone ring (Paulsen, 2002) and they are the most important allergens in the Asteraceae family, present in the oleoresin fraction of leaf, stem, flower and possibly in the pollen. The allergenicity is increased by the presence of an α-methylene group attached to the lactone ring.
3.2.2. Solanaceae species causing allergic contact dermatitis Capsicum annuum (pepper), S. tuberosum (potato) and Solanum lycopersicum (tomato) were the Solanaceae species that were associated to ACD dermatitis with citations of 26, 25 and 14 respectively (Table 1). C. annuum (Sweet, Green or Bell pepper) and Capsicum frutescens (Cayenne or Chili pepper) are 2 peppers of the Solanacea family which are used mainly as vegetables. Urticaria, skin rash and itches were the allergies associated to C. annuum while allergic reactions characterised by urticaria, eczema, atopic dermatitis and itchy skin triggered by exposure to raw, cut potato were reported (Table 1). Exposures to allergen occur during direct contact with potato peelings at home or in food processing plants or after inhalation of potato pollen by farm workers. Studies on the allergens in potato have mainly concentrated on one protein called patatin (Schmidt et al., 2002). This allergen can cause reactions such as eczema and has been implicated in atopic dermatitis. Patatin is sensitive to heat, hence, cooked potatoes no longer have the potential to cause allergic reactions; therefore, potatoes are viewed as ‘safe’ for individuals suffering from food allergies and form the staple food in many countries. Allergic contact dermatitis to tomato was reported as localised and mild itching, irritation, or rash symptoms in the mouth triggered by eating raw tomatoes. The common observation that some people exhibit allergic symptoms to raw tomato is important to the food industry considering the increasing consumption of raw tomatoes in salads worldwide. Ten out of 17 patients (25%) reported allergic reactions to cooked tomatoes; in immunoblotting tests, their sera
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
7
3.2.5. Amaryllidaceae species causing allergic contact dermatitis Amaryllidaceae family members can be recognised easily by their characteristic garlic smell as well as their soft, fleshy leaves. The genus Allium is the most important genus in dermatology and includes many important vegetables such as garlic and onion. Garlic is the only species in the Amaryllidaceae family that was reported for allergic contact dermatitis. All parts of the plant, when damaged, release the potentially irritating and allergenic sap. Diallyl disulfide, allicin, and allyl propyl disulfide have been identified as the principal low molecular weight allergens.
6
No of species
37
5 4 3 2 1 0
Plant families Fig. 2. Plant families implicated in allergic contact dermatitis.
reacted only to lipid transfer protein (LTP) (Pravettoni et al., 2009). In fresh tomato, different LTP isoforms are present and allergenic. 3.2.3. Anarcadiaceae species causing allergic contact dermatitis In the current study, the causes of allergic phytodermatitis in the Anacardeaceae family include M. indica (mango fruit tree), Anacardium occidentale (cashew nut tree) and Smodingium argutum (South African poison ivy) (Table 1). Mango was the most cited (33 citations) cause of ACD in the study area and dermatitis occurs when the sap of the skin, bruised leaf, or stem of the fruit touches the skin. Dermatitis may present as vesicles, dermal lesions or generalised eruptions mostly limited to the angles of the mouth, although the hands may carry the allergens to the eyes and neck. The responsible allergens are urushiol and other sensitising substances include cardol, limonene and Bpinene (Oka et al., 2004). These allergens are found in the stems, leaves, and peel, but not in fruit juice, hence the juice may be drunk by sensitised persons (Wiwanitkit, 2008). Delayed hypersensitivity to mango is CD-4 cells mediated. Allergens in mango sap sensitise CD-4 cells which on repeated exposure migrate towards the epidermis where they release cytokine-damaging keratinocytes, leading to epidermal spongiosis which reaches a peak in 24–72 h, and then slowly subsides. This accounts for the later onset of symptoms in allergic individuals. The African poison ivy (S. argutum) is a Southern African shrub which is monotypic in the genus Smodingium, and was discovered in Pondoland by J. F. Drège during an 1832 expedition with the zoologist Andrew Smith. It is found only in South Africa and there is no other species in the genus. The plant has properties comparable to the American poison ivy, as its sap contains heptadecyl catechols that are toxic to the skin, its immuno-chemical reaction is common in other toxic anacardiaceous species and the rash is very oedematous (Findlay, 1963). The middle layer of cashew nut is filled with a brownish oil rich in cardol and anacardic acid, chemically similar to urushiol. These catechols are destroyed when the nut is properly roasted and processed, but harvesters can develop allergic phytodermatitis from exposure to the oil. 3.2.4. Citrus species causing allergic contact dermatitis Besides its use in the food industry, Citrus spp are used for aromatic oils for perfumery and in the manufacture of soaps and cosmetics. The species associated to ACD in the study area are Citrus sinensis (sweet orange) and Citrus limon (lemon) with 19 and 18 citations respectively (Table 1). Hand dermatitis was reported especially by food handlers. The potential sensitisers in Citrus spp include geraniol, citral and the hydroperoxide derivative of D-limonene, which are usually included in fragrances. The mechanism of sensitisation is currently an object of research.
3.2.6. Capparaceae species causing allergic contact dermatitis The Capparaceae family is regarded as the tropical relative of the mustard family, which comprises some 650 species of small trees and shrubs in 30 genera (Rozas-Muñoz et al., 2012). The species of this family associated to ACD in the study area is Capparis spinosa, or caper bush, a shrub with greyish oval leaves and showy white-pink flowers with several prominent stamens. C. spinosa contains thioglucosides, which are broken down enzymatically, in the presence of water, to isothiocyanates, potent irritants, which appear to be also the most important allergens (Dannaker and White, 1987). Contact dermatitis from this plant was reported as eczematous eruption of the exposed areas of the upper limbs. 3.2.7. Apiaceae species causing allergic contact dermatitis Carrot (Daucus carota) is a root vegetable of usually orange colour which was previously grown for its aromatic leaves and seeds but it is now cultivated mainly for food. Allergic contact dermatitis induced by carrot was reported as hand or finger-tip dermatitis (Table 1). The responsible allergen has been identified as falcarinol, an allergen also present in celery (Apium graveolens L.) (Murdoch and Dempster, 2000). Occupational allergic contact dermatitis induced by carrot is well recognised, particularly affecting employees working in canning factories (Rozas-Muñoz et al., 2012). 3.3. Occupational exposure to plant-induced allergic contact dermatitis Out of the 24 plant species that were mentioned in the survey for causing ACD, 67% are principally used as food (Fig. 3). This finding implies that workers within the food industries (such as bakers, caterers, cooks, chefs, etc.) have a higher-than-average risk of contacting plant-induced ACD. Occupational dermatitis has been frequently reported in the literature. In garlic for example, the typical occupational gesture of cutting the bulb, which is held between the thumb and the first/second finger of the non-dominant hand leads to the characteristic distribution of hyperkeratotic eczema on the tips of the fingers (Ekeowa-Anderson et al., 2007). Allergy occurring soon after contact with rubber latex was reported as blisters, scaling and erythema. Approximately 10% of health personnel who are occupationally exposed to rubber gloves and other rubber
Ornamental 4% Medicinal 8%
Commercial 4% Weed 17%
Food 67%
Fig. 3. Principal uses of plants reported for causing irritant contact dermatitis.
38
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39
articles have a particularly high incidence of allergy to natural rubber latex. Latex is the milky sap of Hevea brasiliensis tree, which is processed to manufacture multiple products, including gloves, condoms and balloons. Latex allergy has been recognised as a very important health problem, due to an increase in frequency, and to its ability to induce severe reactions. The protein content of natural rubber triggers a Type-4 delayed immunological reaction which is extremely itchy and uncomfortable. Although the true prevalence of occupational allergic contact dermatitis in South Africa is not known, a high burden of occupational skin disease will definitely translate into large costs in terms of days lost from work and adjustments necessary in the workplace. Hence, early recognition of allergic contact dermatitis may lead to improved outcomes to both employees and employers. Therefore, health care practitioners need to be aware of possible occupational causes for all cases of ACD.
workplace. Hence, early recognition of allergic contact dermatitis may lead to improved outcomes to both employees and employers. Therefore, health care practitioners need to be aware of possible occupational causes for all cases of ACD. Competing interest The authors declare that there is no conflict of interests regarding the publication of this paper. Authors' contributions WOM designed the study and took part in data collection and analysis, DSG took part in data collection and writing of the manuscript, and AJA took part in writing and editing of the manuscript.
3.4. Cross-reactions to different plant allergens Acknowledgements Allergy to a particular plant rarely presents as an isolated disorder, due to cross-reactivity with similar allergens in other plants. Crossreactivity or cross-sensitisation is a term used to describe a phenomenon where the allergen to which a person is sensitive is present in different plants, resulting in that person being allergic to those different plants. Our immune systems recognise particular antigen structures as foreign without regard to the origin of these molecules. Close structural similarities between any two allergens from divergent sources can produce similar allergic reactions in sensitive individuals. Two patterns of associated allergies were identified among the plants implicated for ACD in the current study: mango plant allergy with celery, carrot, tomato, papaya and banana and rubber latex allergy with banana, pepper and potato, a condition known as the latex-fruit syndrome. Allergens responsible for this syndrome seem to be a group of shared plant proteins, to which patients react. This cross reactivity is attributed to the fact that multiple antigens can bind to an immunoglobulin E (IgE) antibody at corresponding sites resulting to an immune response. For example, several types of proteins have been identified as being involved in the latex-fruit syndrome such as class I chitinases (Rozynek et al., 2006) from banana containing an N-terminal heveinlike domain which cross-reacts with hevein (Hev b6.02), a major IgE allergen for patients allergic to natural rubber latex. Other important natural rubber latex-allergens are Hev b 2 (which shows crossreactivity with proteins of bell pepper) and Hev b 7, a patatin-like protein (cross-reacts with its homologous protein in potato). These proteins seem to be inactivated by heating, which could explain why some plant foods that contain these allergens are not associated with this syndrome when consumed after cooking. 3.5. Conclusion The current study was undertaken to investigate and document plants responsible for allergic contact dermatitis (ACD) in the Eastern Cape. Twenty four plant species distributed in 11 families were reported as causative agents of ACD. The most representative families were Asteraceae, Solanaceae, Anarcadiaceae and Rutaceae. Herbs constituted 62.50%, trees 25.0% and shrubs 12.50%. The Asteraceae was the most important allergenic plant family, represented by the highest number of species. Mango (Mangifera indica) was the most cited cause of ACD in the study area. Two patterns of associated allergies were identified among the plants implicated for ACD in the current study: mango plant allergy with celery, carrot, tomato, papaya and banana and rubber latex allergy with banana, pepper and potato. Out of the 24 plant species that were mentioned in the survey for causing ACD, 67% are principally used as food. Although the true prevalence of occupational allergic contact dermatitis in South Africa is not known, a high burden of occupational skin disease will definitely translate into large costs in terms of days lost from work and adjustments necessary in the
The authors greatly appreciate the National Research Foundation (NRF) (grant no. T304) and Govan Mbeki Research and Development Centre (GMRDC) of the University of Fort Hare, South Africa (grant no. C295) for financing this study. References Abbasi, A.M., Khan, M.A., Ahmad, M., Zafar, M., Jahan, S., Sultana, S., 2010. Ethnopharmacological application of medicinal plants to cure skin diseases and in folk cosmetics among the tribal communities of North-West Frontier Province. Pakistan Journal of Ethnopharmacology 128, 322–335. Akoto, O., Oppong, I.V., Addae-Mensah, I., Waibel, R., Achenbach, H., 2008. Isolation and characterization of dipeptide derivative and phytosterol from Capparis tomentosa Lam. Scientifc Research and Essays 3, 355–358. Anderson, C., Lis-Balchin, M., Kirk-Smith, M., 2000. Evaluation of massage with essential oils on childhood atopic eczema. Phytotherapy Research 14, 452–456. Ben-Shoshan, M., Turnbull, E., Clarke, A., 2012. Food allergy: temporal trends and determinants. Current Allergy and Asthma Reports 12, 346–372. Bhat, R.B., Jacobs, T.V., 1985. Traditional herbal medicine in Transkei. Journal of Ethnopharmacology 48, 7–12. Bilsland, D., Strong, A., 1990. Allergic contact dermatitis from the essential oil of French marigold (Tagetes patula) in an aromatherapist. Contact Dermatitis 23, 55–56. Dannaker, C.J., White, I.R., 1987. Cutaneous allergy to mustard in a salad maker. Contact Dermatitis 16, 212–214. Dold, A.P., Cocks, M.L., 2000. Indigenous plant use of the amaXhosa people on the Eastern border of the Great Fish River Reserve, Eastern Cape. Annals of the Eastern Cape Museum 1, 26–53. Ekeowa-Anderson, A.L., Shergil, B., Goldsmith, P., 2007. Allergic contact cheilitis to garlic. Contact Dermatitis 56, 174–175. Findlay, G.H., 1963. Dermatitis of ‘poison ivy’ type from an indigenous South African Plant —Smodingium argutum E. Mey. (Anacardiaceae). South African Medical Journal 37, 883–888. Grierson, D.S., Afolayan, A.J., 1999. Antibacterial activity of some indigenous plants used for the treatment of wounds in the Eastern Cape, South Africa. Journal of Ethnopharmacology 66, 103–106. Hausen, B.M., Helmke, B., 1995. Butenylbithiophene, alpha-terthienyl and hydroxytremetone as contact allergens in cultivars of marigold (Tagetes sp.). Contact Dermatitis 33, 33–37. Hay, R., Marks, R., 2004. The International Foundation for Dermatology: an exemplar of the increasingly diverse activities of the International League of Dermatological Societies. British Journal of Dermatology 150, 747–749. Jack, A.R., Norris, P.L., Storrs, S.J., 2013. Allergic contact dermatitis to plant extracts in cosmetics. Seminars in Cutaneous Medicine and Surgery 32, 140–146. Modi, G.M., Doherty, C.B., Katta, R., Orengo, I.F., 2009. Irritant contact dermatitis from plants. Dermatitis 20, 63–78. Murdoch, S.R., Dempster, J., 2000. Allergic contact dermatitis from carrot. Contact Dermatitis 42, 236. Oka, K., Saito, F., Yasuhara, T., Sugimoto, A., 2004. A study of cross reactions between mango contact allergens and urushiol. Contact Dermatitis 5, 292–296. Paulsen, E., 2002. Contact sensitization from Compositae-containing herbal remedies and cosmetics. Contact Dermatitis 47, 189–198. Phillips, O., Gentry, A.H., Reynel, C., Wilkin, P., Gálvez- Durand, C., 1994. Quantitative ethnobotany and Amazonian conservation. Conservation Biology 8, 225–248. Phillipson, P.B., 1987. A checklist of vascular plants of the Amatole Mountains, Eastern Cape Province: Ciskei. Bothalia 17237–17256. Pravettoni, V., Primavesi, L., Farioli, L., Brenna, O.V., Pompei, C., Conti, A., Scibilia, J., Piantanida, M., Mascheri, A., Pastorello, E.A., 2009. Tomato allergy: detection of IgEbinding lipid transfer proteins in tomato derivatives and in fresh tomato peel, pulp, and seeds. Journal of Agriculture and Food Chemistry 57, 10749–10754.
W.M. Otang et al. / South African Journal of Botany 97 (2015) 32–39 Rozas-Muñoz, E., Lepoittevin, J.P., Pujol, R.M., Giménez-Arnau, A., 2012. Allergic contact dermatitis to plants: understanding the chemistry will help our diagnostic approach. Actas Dermosifiliograficas 103, 456–477. Rozynek, P., Rihs, H.P., Gaspar, A., Brüning, T., Raulf-Heimsoth, M., 2006. The new Hev b 7.02 iso-allergen from Hevea brasiliensis is an important allergen for health care workers and spina bifida patients. Allergy 61, 508–509. Saint-Mezard, P., Rosieres, A., krasteva, M., Berard, F., Dubois, B., kaiserlian, D., Nicolas, J., 2004. Allergic contact dermatitis. European Journal of Dermatology 14, 284–295.
39
Sasseville, D., 1999. Phytodermatitis. Journal of Cutaneous Medicine and Surgery 3, 263–279. Schmidt, M.H., Raulf-Heimsoth, M., Posch, A., 2002. Evaluation of patatin as a major crossreactive allergen in latex-induced potato allergy. Allergy 146, 131–135. van Ketel, W.G., 1975. A cauliflower allergy. Contact Dermatitis 1, 324–325. Wiwanitkit, V., 2008. Mango dermatitis. Indian Journal of Dermatology 53, 158.