Phytophotodermatitis

Phytophotodermatitis
Other names: Berloque dermatitis,[1][2][3] margarita photodermatitis[4][5]
Phytophotodermatitis caused by lime
SpecialtyDermatology

Phytophotodermatitis is a phototoxic inflammatory reaction of the skin resulting from contact with a light-sensitizing botanical agent followed by exposure to ultraviolet light (from the sun, for instance). Symptoms include erythema, edema, blisters (vesicles and/or bullae), and delayed hyperpigmentation. Heat and moisture tend to exacerbate the reaction.

A reaction may be elicited in any person who has been exposed to adequate amounts of both a Photosensitizer agent and ultraviolet light. Phytophotodermatitis is not an immunologic response; no prior exposure to the photosensitizing agent is required.

The photosensitizing substances found in phototoxic plants belong to a class of chemical compounds called the furanocoumarins, which are activated by long-wavelength ultraviolet (UVA) light. The most toxic of these organic compounds are the linear furanocoumarins, so called since they exhibit a linear chemical structure. Bergapten and xanthotoxin (also known as methoxsalen), two linear furanocoumarins derived from psoralen, are invariably found in plants associated with phytophotodermatitis.[2]

Signs and symptoms

A reaction typically begins within 24 hours of exposure and peaks at 48–72 hours after exposure.[6] Initially, the skin turns red and starts to itch and burn. Large blisters (or bullae) form within 48 hours.[7] The blisters may leave black, brown, or purplish scars that can last for several years. This hyperpigmentation of the skin is caused by the production of melanin triggered by the furanocoumarins.

Although media reports have suggested that eye exposure to the agent can lead to temporary or permanent blindness, the risk of permanent blindness is not supported by existing research.[8]

Phytophotodermatitis can affect people of any age. In children, it has been mistaken for child abuse.[9]

  • Phytophotodermatitis
    Phytophotodermatitis
  • Phytophotodermatitis
    Phytophotodermatitis
  • A severe case of phytophotodermatitis in an 11-year-old boy.
    A severe case of phytophotodermatitis in an 11-year-old boy.

Phototoxic species

Plants associated with phytophotodermatitis mainly come from four plant families:[2][10] the carrot family (Apiaceae), the citrus family (Rutaceae), the mulberry family (Moraceae), and the legume family (Fabaceae).

Apiaceae

The carrot family Apiaceae (or Umbelliferae) is the main family of plants associated with phytophotodermatitis. Of all the plant species that have been reported to induce phytophotodermatitis, approximately half belong to the family Apiaceae.[11]

False bishop's weed (Ammi majus), the world's major source of the linear furanocoumarin xanthotoxin, has been used since antiquity to treat vitiligo[2] but accidental or inappropriate use of this plant can lead to phytophotodermatitis.[12] Despite this danger, A. majus continues to be cultivated for its furanocoumarins,[13] which are still used for the treatment of skin disease.

Numerous species in the family Apiaceae are cultivated as food products, some of which exhibit phototoxic effects. In particular, celery, parsnip, and parsley have been reported to cause phytophotodermatitis among agricultural workers, grocery workers, and other occupational food handlers.[14][15][16][17][18][19][2]

A number of phototoxic plant species in the carrot family have become invasive species, including wild parsnip (Pastinaca sativa)[20][21] and the tall hogweeds of the genus Heracleum,[22][23] namely, Persian hogweed (Heracleum persicum), Sosnowsky's hogweed (Heracleum sosnowskyi), and giant hogweed (Heracleum mantegazzianum). In particular, the public health risks of giant hogweed are well known.[24]

Other plant species in the family Apiaceae that are associated with phytophotodermatitis include blister bush (Notobubon galbanum), cow parsley (Anthriscus sylvestris), wild carrot (Daucus carota), various species of the genus Angelica (e.g., Korean angelica Angelica gigas), and most (if not all) species of the genus Heracleum (esp. the tall invasive hogweeds and the cow parsnips, Heracleum sphondylium and Heracleum maximum).

Rutaceae

The citrus family Rutaceae is the second most widely distributed family of plants associated with phytophotodermatitis.

Effect of common rue on skin

Numerous citrus fruits in the family Rutaceae exhibit phototoxic effects. Of these, perhaps the best known is lime.[25][26][27][28] Phytophotodermatitis associated with limes is sometimes colloquially referred to as "lime disease,"[29][30] not to be confused with Lyme disease.

In the family Rutaceae, the most severe reactions are caused by the essential oil of the bergamot orange (Citrus bergamia).[2][31] Bergamot essential oil has a higher concentration of bergapten (3000–3600 mg/kg) than any other citrus-based essential oil, even lime oil, which contains 1700–3300 mg/kg of bergapten.[32]

Other plant species in the family Rutaceae that are associated with phytophotodermatitis include burning bush (Dictamnus albus),[33] common rue (Ruta graveolens),[34][35][36][37] and other plants in the genus Ruta.

Moraceae

The mulberry family Moraceae is often associated with phytophotodermatitis. Multiple species in the genus Ficus are known to exhibit phototoxic effects. Of these, the common fig (Ficus carica) is well known and thoroughly documented.

Like Ammi majus in the family Apiaceae, the common fig has been used since antiquity to treat vitiligo[38] but the milky sap of fig leaves can cause phytophotodermatitis if used accidentally or inappropriately.[39][40][41][42][43][44] A literature search revealed 19 cases of fig leaf-induced phytophotodermatitis reported between 1984 and 2012.[44] In Brazil, several hospitals reported more than 50 cases of fig leaf-induced burn in one summer.[43] In most cases, patients reportedly used the leaves of the fig plant for folk remedies, tanning, or gardening.

Other plant species in the family Moraceae that are associated with phytophotodermatitis include Ficus pumila[45][46] and Brosimum gaudichaudii.[47] Like Ficus carica, the South American species Brosimum gaudichaudii has been shown to contain both psoralen and bergapten.

Prevention

The first and best line of defense against phytophotodermatitis is to avoid contact with phototoxic substances in the first place:

  • Avoid contact with the plant family Apiaceae, citrus fruits, and other biological agents known to have phototoxic effects. Do not incinerate phototoxic plants and agents since this will serve to disperse the phototoxic substances more widely.[48]
  • In outdoor situations where contact with phototoxic plants is likely, wear long pants and a long-sleeve shirt. Wear gloves and protective eyewear before handling such plants.
  • If protective clothing is not available, apply sunscreen to exposed areas. This will provide some measure of protection if contact is made.
  • After an outdoor activity, take a shower or a bath as soon as possible. Wash your clothing and then wash your hands after handling the dirty clothes.

A second line of defense is to avoid sunlight, so as not to activate a phototoxic substance:

  • If you come in contact with a phototoxic substance, immediately wash the affected area with soap and cold water, and avoid any further exposure to sunlight for at least 48 hours. Heat and moisture can worsen the skin reaction,[24] which is why it’s important to wash the affected area with soap and cold water.
  • Stay indoors, if possible. Be sure to avoid light shining through windows.
  • If staying indoors is not an option, cover the affected area with sun protective clothing.
  • In lieu of sun-protective clothing, apply sunscreen[49] to the affected areas after washing.

Phytophotodermatitis is triggered by long wavelength ultraviolet light (called UVA) in the range of 320–380 nanometers,[6] so the best sun-protective clothing and sunscreen products will block these wavelengths of UVA radiation.

In 2011, the U.S. Food and Drug Administration (FDA) established a "broad spectrum" test for determining a sunscreen product's UVA protection.[50] Sunscreen products that pass the test are allowed to be labeled as "Broad Spectrum" sunscreens, which protect against both UVA and UVB rays.

There is no equivalent test or FDA-approved labeling for sun-protective clothing. Some clothing is labeled with an Ultraviolet Protection Factor (UPF) but test results from Consumer Reports[51] suggest that UPF is an unreliable indicator of UV protection.

Treatment

Many different topical and oral medications may be used to treat the inflammatory reaction of phytophotodermatitis. A dermatologist may also prescribe a bleaching cream to help treat the hyperpigmentation and return the skin pigmentation back to normal. If the patient does not receive treatment, the affected sites may develop permanent hyperpigmentation or hypopigmentation.[6]

History

The photosensitizing effects of plants have been known since antiquity. In Egypt around 2000 B.C., the juice of Ammi majus "was rubbed on patches of vitiligo after which patients were encouraged to lie in the sun."[2] In A.D. 50, the Greek physician Dioscorides observed that pigment would return to patches of vitiligo if "cataplasmed with ye leaves or ye boughes of ye Black Figge,"[38] an apparent reference to Ficus carica, the common fig. These ancient practices acknowledged the hyperpigmentation effects now known to accompany phytophotodermatitis.

One of the earliest reports of plant-based dermatitis was given by Chaumton in 1815, who noted that the outer rind and root of cow parsnip (a common name for any Heracleum species of plant) contained an acrid sap sufficiently strong to inflame and ulcerate the skin.[52] Similarly in 1887 Sornevin reported that Heracleum sphondylium caused dermatitis. However, neither of these early reports recognized the crucial role of ultraviolet radiation.

"Berloque dermatitis"[3] (from the French word "berloque" meaning trinket or charm) is a term coined by Rosenthal in 1925 to describe the pendant-like streaks of pigmentation observed on the neck, face, and arms of patients.[53][2] He was unaware that, in 1916, Freund had correctly observed that these pigmentation effects were due to sun exposure after the use of Eau de Cologne, a perfume infused with bergamot oil.[54] It is now known that bergamot oil contains a significant amount of bergapten,[2] a linear furanocoumarin that gets its name from the bergamot orange.

In 1937, dermatitis from Heracleum mantegazzianum was reported by Miescher and Burckhardt who suspected the possibility of light sensitization.[55] A few years later, Kuske confirmed this hypothesis.[56][57] In 1942, Klaber introduced the term "phytophotodermatitis" to emphasize that both plants and light were required to affect a reaction.[58][28]

Darrell Wilkinson, a British dermatologist, gave an accurate description of the disease in the 1950s.[59] In 1961, Efremov reported 357 cases of phytophotodermatitis from Heracleum dulce (sweet cow parsnip). He "noted the requirement for sunlight in evoking the dermatitis since inunction of the juice of the plant without exposure to sunlight was harmless."[60] Between 1962 and 1976, numerous reports of phytophotodermatitis from giant hogweed (Heracleum mantegazzianum) were reported. By 1980, the photosensitizing effects of various plant species had become well known (as evidenced by the comprehensive work of Mitchell and Rook[61]).

See also

References

  1. ↑ James WD, Berger TG, Elston DM, eds. (2006). Andrews' Diseases of the Skin: Clinical Dermatology. Saunders Elsevier. p. 32. ISBN 978-0-7216-2921-6.
  2. 1 2 3 4 5 6 7 8 9 McGovern TW, Barkley TM (2000). "Botanical Dermatology". The Electronic Textbook of Dermatology. Internet Dermatology Society. 37 (5). Section Phytophotodermatitis. doi:10.1046/j.1365-4362.1998.00385.x. PMID 9620476. Archived from the original on June 1, 2017. Retrieved November 29, 2018.
  3. 1 2 Alikhan A (March 4, 2016). "Berloque Dermatitis". Medscape. Archived from the original on November 26, 2020. Retrieved August 9, 2018.
  4. ↑ Riahi RR, Cohen PR, Robinson FW, Gray JM (June 2009). "What Caused The Rash On This Man's Wrist And Hand?". The Dermatologist. 11 (6). Archived from the original on 2020-10-22. Retrieved 2021-05-06.
  5. ↑ Abramowitz AI, Resnik KS, Cohen KR (March 1993). "Margarita photodermatitis". The New England Journal of Medicine. 328 (12): 891. doi:10.1056/NEJM199303253281220. PMID 8441448.
  6. 1 2 3 Baugh WP (September 8, 2016). "Phytophotodermatitis". Medscape. Archived from the original on November 26, 2020. Retrieved August 9, 2018.
  7. ↑ Solis RR, Dotson DA, Trizna Z (2000). "Phytophotodermatitis: a sometimes difficult diagnosis". Archives of Family Medicine. 9 (10): 1195–6. doi:10.1001/archfami.9.10.1195. PMID 11115230.
  8. ↑ "Giant Hogweed" (PDF). Peterborough, Ont.: Ministry of Natural Resources and Forestry, Government of Ontario. p. 2. Archived (PDF) from the original on June 10, 2019. Retrieved July 15, 2018.
  9. ↑ Barradell R, Addo A, McDonagh AJ, Cork MJ, Wales JK (April 1993). "Phytophotodermatitis mimicking child abuse". European Journal of Pediatrics. 152 (4): 291–2. doi:10.1007/BF01956735. PMID 8482273. S2CID 11778627.
  10. ↑ Kavli G, Volden G (April 1984). "Phytophotodermatitis". Photo-Dermatology. 1 (2): 65–75. PMID 6397734.
  11. ↑ Pathak MA, Daniels Jr F, Fitzpatrick TB (September 1962). "The Presently Known Distribution of Furocoumarins (Psoralens) in Plants". Journal of Investigative Dermatology. 39 (3): 225–239. doi:10.1038/jid.1962.106. PMID 13941836.
  12. ↑ Alouani I, Fihmi N, Zizi N, Dikhaye S (2018). "Phytophotodermatitis following the use of Ammi Majus Linn (Bishop's weed) for vitiligo". Our Dermatol. Online. 9 (1): 93–94. doi:10.7241/ourd.20181.29.
  13. ↑ "Plants For A Future: Ammi majus". Archived from the original on 2011-06-05. Retrieved 2021-05-06.
  14. ↑ Birmingham DJ, Key MM, Tublich GE, Perone VB (1961). "Phototoxic bullae among celery harvesters". Arch Dermatol. 83 (1): 73–87. doi:10.1001/archderm.1961.01580070079008. Cited in McGovern and Barkley 2000, section Phytophotodermatitis Archived 2012-02-14 at the Wayback Machine.
  15. ↑ Centers for Disease Control (CDC) (January 1985). "Phytophotodermatitis among grocery workers--Ohio". MMWR. Morbidity and Mortality Weekly Report. 34 (1): 11–3. PMID 3155560. Archived from the original on 2020-11-26. Retrieved 2021-05-06.
  16. ↑ Berkley SF, Hightower AW, Beier RC, Fleming DW, Brokopp CD, Ivie GW, Broome CV (September 1986). "Dermatitis in grocery workers associated with high natural concentrations of furanocoumarins in celery". Annals of Internal Medicine. 105 (3): 351–5. doi:10.7326/0003-4819-105-3-351. PMID 2943201.
  17. ↑ Aberer W (January 1992). "Occupational dermatitis from organically grown parsnip (Pastinaca sativa L.)". Contact Dermatitis. 26 (1): 62. doi:10.1111/j.1600-0536.1992.tb00880.x. PMID 1534739.
  18. ↑ Lovell CR (1993). Plants and the skin (1st ed.). Oxford: Blackwell Scientific Publications. Cited in McGovern and Barkley 2000, section Phytophotodermatitis Archived 2012-02-14 at the Wayback Machine.
  19. ↑ Lutchman L, Inyang V, Hodgkinson D (November 1999). "Phytophotodermatitis associated with parsnip picking". Journal of Accident & Emergency Medicine. 16 (6): 453–4. doi:10.1136/emj.16.6.453. PMC 1343418. PMID 10572825.
  20. ↑ Averill KM, Di'Tommaso A (2007). "Wild parsnip (Pastinaca sativa): A troublesome species of increasing concern" (PDF). Weed Technology. 21: 279–287. doi:10.1614/WT-05-186.1. S2CID 86774319. Archived (PDF) from the original on 2020-11-26. Retrieved 2021-05-06.
  21. ↑ Cain N, Darbyshire SJ, Francis A, Nurse RE, Simard M (2010). "The Biology of Canadian weeds. 144. Pastinaca sativa L." Can. J. Plant Sci. 90 (2): 217–240. doi:10.4141/CJPS09110.
  22. ↑ Booy O, Cock M, Eckstein L, Hansen SO, Hattendorf J, Hüls J, Jahodová S, Krinke L, Marovoková L, Müllerová J, Nentwig W, Nielsen C, Otte A, Pergl J, Perglová I, Priekule I, Pusek P, Ravn HP, Thiele J, Trybush S, Wittenberg R (2005). The giant hogweed best practice manual: guidelines for the management and control of invasive weeds in Europe (PDF). Hørsholm: Center for Skov, Landskab og Planlægning/Københavns Universitet. ISBN 87-7903-209-5. Archived (PDF) from the original on November 26, 2020. Retrieved September 1, 2018.
  23. ↑ MacDonald F, Anderson H (May 2012). "Giant Hogweed (Heracleum mantegazzianum): Best Management Practices in Ontario" (PDF). Ontario Invasive Plant Council, Peterborough, ON. Archived (PDF) from the original on June 22, 2017. Retrieved September 1, 2018.
  24. 1 2 "Health Hazards & Safety Instructions for Giant Hogweed (with graphic photos)". New York State Department of Environmental Conservation. Archived from the original on November 12, 2020. Retrieved September 3, 2018.
  25. ↑ Gross TP, Ratner L, de Rodriguez O, Farrel KP, Israel E (March 1987). "An outbreak of phototoxic dermatitis due to limes". American Journal of Epidemiology. 125 (3): 509–14. doi:10.1093/oxfordjournals.aje.a114557. PMID 3812457.
  26. ↑ Kung AC, Stephens MB, Darling T (June 2009). "Phytophotodermatitis: bulla formation and hyperpigmentation during spring break" (PDF). Military Medicine. 174 (6): 657–61. doi:10.7205/milmed-d-01-7208. PMID 19585784. Archived from the original on 2021-08-28. Retrieved 2021-05-06.
  27. ↑ Hankinson A, Lloyd B, Alweis R (2014). "Lime-induced phytophotodermatitis". Journal of Community Hospital Internal Medicine Perspectives. 4 (4): 25090. doi:10.3402/jchimp.v4.25090. PMC 4185147. PMID 25317269.
  28. 1 2 de Almeida Junior HL, Sartori DS, Jorge VM, Rocha NM, de Castro LA (2016). "Phytophotodermatitis: A Review of Its Clinical and Pathogenic Aspects". Journal of Dermatological Research. 1 (3): 51–56. doi:10.17554/j.issn.2413-8223.2016.01.15.
  29. ↑ "Lime Disease: How a Fruity Drink Can Give You a Rash". SciShow. July 24, 2017. Archived from the original on August 28, 2021. Retrieved November 5, 2018.
  30. ↑ Weber IC, Davis CP, Greeson DM (1999). "Phytophotodermatitis: the other "lime" disease". The Journal of Emergency Medicine. 17 (2): 235–7. doi:10.1016/S0736-4679(98)00159-0. PMID 10195477.
  31. ↑ Kaddu S, Kerl H, Wolf P (2001). "Accidental bullous phototoxic reactions to bergamot aromatherapy oil". J Am Acad Dermatol. 45 (3): 458–461. doi:10.1067/mjd.2001.116226. PMID 11511848. Cited in CIR 2013 Archived 2019-07-28 at the Wayback Machine.
  32. ↑ "Toxicological Assessment of Furocoumarins in Foodstuffs" (PDF). The German Research Foundation (DFG). DFG Senate Commission on Food Safety (SKLM). 2004. Archived (PDF) from the original on December 24, 2019. Retrieved November 1, 2018.
  33. ↑ Schempp CM, Sonntag M, Schöpf E, Simon JC (September 1996). "Dermatitis bullosa striata pratensis caused by Dictamnus albus L. (burning bush)". Hautarzt (in German). 47 (9): 708–710. doi:10.1007/s001050050494. PMID 8999028. S2CID 23601334.{{cite journal}}: CS1 maint: unrecognized language (link)
  34. ↑ Wessner D, Hofmann H, Ring J (October 1999). "Phytophotodermatitis due to Ruta graveolens applied as protection against evil spells". Contact Dermatitis. 41 (4): 232. doi:10.1111/j.1600-0536.1999.tb06145.x. PMID 10515113.
  35. ↑ Furniss D, Adams T (2007). "Herb of grace: an unusual cause of phytophotodermatitis mimicking burn injury". Journal of Burn Care & Research. 28 (5): 767–9. doi:10.1097/BCR.0B013E318148CB82. PMID 17667834.
  36. ↑ Eickhorst K, Deleo V, Csaposs J (March 2007). "Rue the herb: Ruta graveolens--associated phytophototoxicity". Dermatitis. 18 (1): 52–5. doi:10.2310/6620.2007.06033. PMID 17303046.
  37. ↑ Arias-Santiago SA, Fernández-Pugnaire MA, Almazán-Fernández FM, Serrano-Falcón C, Serrano-Ortega S (November 2009). "Phytophotodermatitis due to Ruta graveolens prescribed for fibromyalgia". Rheumatology. 48 (11): 1401. doi:10.1093/rheumatology/kep234. PMID 19671699.
  38. 1 2 Mitchell J, Rook A (1979). Botanical Dermatology: Plants and Plant Products Injurious to the Skin. Vancouver: Greengrass. Cited in McGovern and Barkley 2000, section Phytophotodermatitis Archived 2012-02-14 at the Wayback Machine.
  39. ↑ Bollero D, Stella M, Rivolin A, Cassano P, Risso D, Vanzetti M (November 2001). "Fig leaf tanning lotion and sun-related burns: case reports". Burns. 27 (7): 777–779. doi:10.1016/S0305-4179(01)00033-X. PMID 11600261.
  40. ↑ Derraik JG, Rademaker M (2007). "Phytophotodermatitis caused by contact with a fig tree (Ficus carica)". N Z Med J. 120 (1261): U2720. PMID 17867224.
  41. ↑ Polat M, Öztaş P, Dikilitaş MC, Allı N (December 2008). "Phytophotodermatitis due to Ficus carica". Dermatol Online J. 14 (12): 9. PMID 19265622. Archived from the original on 2021-04-10. Retrieved 2021-05-06.
  42. ↑ Zhang R, Zhu W (2011). "Phytophotodermatitis due to Chinese herbal medicine decoction". Indian J Dermatol. 56 (3): 329–331. doi:10.4103/0019-5154.82498. PMC 3132918. PMID 21772602.
  43. 1 2 Sforza M, Andjelkov K, Zaccheddu R (July 2013). "Severe burn on 81% of body surface after sun tanning". Turkish Journal of Trauma and Emergency Surgery. 19 (4): 383–384. doi:10.5505/tjtes.2013.44522. PMID 23884685.
  44. 1 2 Son JH, Jin H, You HS, Shim WH, Kim JM, Kim GW, Kim HS, Ko HC, Kim MB, Kim BS (February 2017). "Five Cases of Phytophotodermatitis Caused by Fig Leaves and Relevant Literature Review". Annals of Dermatology. 29 (1): 86–90. doi:10.5021/ad.2017.29.1.86. PMC 5318534. PMID 28223753.
  45. ↑ English PB, Grey LP (June 1943). "Sap dermatitis and conjunctivitis caused by the wild fig (Ficus pumila)". Medical Journal of Australia. 1 (26): 578–579. doi:10.5694/j.1326-5377.1943.tb44690.x. Cited in Mitchell and Rook 1979.
  46. ↑ Rademaker M, Derraik JG (July 2012). "Phytophotodermatitis caused by Ficus pumila". Contact Dermatitis. 67 (1): 53–56. doi:10.1111/j.1600-0536.2012.02026.x. PMID 22681467.
  47. ↑ Martins JE, Pozetti GL, Sodré M (1974). "Effects of psoralen and bergapten on irradiated skin". Int J Dermatol. 13 (3): 124–128. doi:10.1111/j.1365-4362.1974.tb01781.x. PMID 4836605.
  48. ↑ Davis D (August 12, 2011). "Sun-related Skin Condition Triggered by Chemicals in Certain Plants, Fruits". Dermatology, Mayo Clinic. Archived from the original on November 26, 2020. Retrieved August 8, 2018.
  49. ↑ Leonard J (August 19, 2017). "Phytophotodermatitis: When plants and light affect the skin". Medical News Today. Archived from the original on September 4, 2019. Retrieved August 8, 2018.
  50. ↑ "FDA announces new requirements for over-the-counter (OTC) sunscreen products marketed in the U.S." U.S. Food and Drug Administration. June 11, 2011. Archived from the original on April 23, 2019. Retrieved August 9, 2018.
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  52. ↑ Chaumton, FP (1815). Flore Med Paris. 2: 32. Cited by Mitchell and Rook (1979), p. 692.
  53. ↑ Rosenthal O (1925). "Berloque dermatitis: Berliner Dermatologische". Dermatologische Zeitschrift. 42: 295. doi:10.1159/000250611. Cited in Alikhan 2016.
  54. ↑ Freund E (1916). "Uber bisher noch nicht beschriebene kunstliche Hautverfarbungen". Dermatol Wochenschrift. 63: 931–933. Cited in McGovern and Barkley 2000, section Phytophotodermatitis Archived 2012-02-14 at the Wayback Machine.
  55. ↑ Miescher G, Burckhardt W (1937). "Herakleum Dermatitis: Case Presentation". Schweizer Medizinische Wochenschriff. 67: 82. Cited by Mitchell and Rook (1979), p. 696.
  56. ↑ Kuske H. "Experimental investigations on photodermatitis caused by plant juices". Archiv für Dermatologie und Syphilis. 178: 273. Cited by Mitchell and Rook (1979), p. 696.
  57. ↑ Kuske H (1940). "Perkutane Photosensibilisierung durch pflanzliche Wirkstoffe". Dermatology. 82 (5–6): 273. doi:10.1159/000253838. Cited by Mitchell and Rook (1979), p. 696.
  58. ↑ Klaber R (1942). "Phytophotodermatitis". Br. J. Dermatol. 54 (7): 193–211. doi:10.1111/j.1365-2133.1942.tb10682.x. Cited by McGovern and Barkley, section Phytophotodermatitis Archived 2012-02-14 at the Wayback Machine.
  59. ↑ "Munks Roll Details for Peter Edward Darrell Sheldon Wilkinson". munksroll.rcplondon.ac.uk. Archived from the original on 2017-11-10. Retrieved 2017-11-10.
  60. ↑ Efremov AI. "The Photodermatitis caused by Sweet Cow Parsnip (Heracleum dulce)". Vestn. Derm. Vener. (in Russian). 4: 64.{{cite journal}}: CS1 maint: unrecognized language (link) Cited by Mitchell and Rook (1979), p. 693.
  61. ↑ Mitchell J, Rook A (1979). Botanical Dermatology: Plants and Plant Products Injurious to the Skin. Vancouver: Greengrass.
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