Possible Relation of Tunisian Pemphigus with Traditional Cosmetics: A Multicenter Case-Control Study
Sylvie Bastuji-Garin1,
Hamida Turki2,
Inçaf Mokhtar3,
Rafia Nouira4,
Bassima Fazaa3,
Bechir Jomaa4,
Abdelmajid Zahaf2,
Amel Ben Osman5,
Rafika Souissi6,
Denis Hémon7,
Jean-Claude Roujeau8 and
Mohamed R. Kamoun3
1 Department of Public Health, hôpital Henri Mondor (AP-HP), Université Paris XII, Créteil, France.
2 Department of Dermatology, hôpital H. Chaker, Sfax, Tunisia.
3 Department of Dermatology, hôpital C. Nicolle, Tunis, Tunisia.
4 Department of Dermatology, hôpital F. Hached, Sousse, Tunisia.
5 Department of Dermatology, hôpital H. Thameur, Tunis, Tunisia.
6 Department of Dermatology, hôpital E. Conseil, Tunis, Tunisia.
7 Research Unit in Environmental Epidemiology INSERM U170, Villejuif, France.
8 Department of Dermatology, hôpital Henri Mondor (AP-HP), Université Paris XII, Créteil, France.
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ABSTRACT
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Pemphigus is a severe, autoimmune, blistering disorder with a high incidence among young women in rural Tunisia. The authors investigated explanatory environmental factors. A multicenter case-control study was conducted prospectively from 1992 to 1996 in Tunisia. Sixty-eight incident female cases of pemphigus and 166 controls matched on age, hospital, and geographic area were included. Data collected concerned socioeconomic status, medical history, drug intakes, lifestyle, and environment. Several factors were significantly associated with pemphigus in multivariate logistic regression analyses: traditional cosmetics (odds ratio (OR) = 4.0, 95% confidence interval (CI): 1.1, 14.8); Turkish baths (OR = 3.2, 95% CI: 1.4, 7.3); cutting up raw poultry (OR = 5.1, 95% CI: 1.3, 19.4); contact with ruminants (OR = 2.7, 95% CI: 1.3, 5.8); and wasp, bee, and spider stings (OR = 3.1, 95% CI: 1.5, 6.4). A dose-dependent relation was observed for traditional cosmetics. All risks except insect bites were higher when analysis was restricted to younger women, the demographic group with higher incidence. The strength of the associations, the dose-dependent relation for traditional cosmetics, and the increase of risk estimates for younger women support a causal relation. Traditional cosmetics widely used by Tunisian women could play a major role in excess of cases of pemphigus.
case-control studies; cosmetics; environmental exposures; pemphigus; risk factors; women
Abbreviations:
CI, confidence interval; OR, odds ratio; SD, standard deviation
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INTRODUCTION
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Pemphigus is an autoimmune, mucocutaneous, blistering disease characterized by a loss of epidermal cell-to-cell adhesion (acantholysis) provoked by autoantibodies directed against antigens of the cell surface of keratinocytes (1
). Two distinct forms exist: pemphigus vulgaris, with a suprabasal acantholysis, and pemphigus foliaceus, with acantholysis in the upper parts of the epidermis. Clinically, the acantholysis causes cutaneous blisters and erosions that can be localized or generalized and/or mucosal erosions. Pemphigus is a severe chronic disorder with a mortality rate of about 10 percent and a rather high morbidity due to treatment with high doses of corticosteroids (2
, 3
). Most cases occur sporadically throughout the world. The incidence rates have been estimated to vary from 0.8 to 34 per million inhabitants per year, depending on geographic and ethnic factors (4
). In North America and Europe, pemphigus vulgaris is the most common type, affecting men and women equally after the fourth decade generally, with an incidence rate from one to three per million inhabitants (4
). In South America, pemphigus foliaceus (named fogo selvagem) is endemic, with as many as 34 incident cases per million inhabitants in rural areas of Brazil, affecting children and young adults of both sexes, with a peak incidence in the second and third decade (5
, 6
).
The cause of the disease remains unknown, but the great variations of incidence rates, clinical features, and demographic characteristics among countries lead to a suspicion of different risk factors (4
). A strong association of the class II genes with pemphigus has been demonstrated (4
). In North America and Europe, several drugs have been reported to induce pemphigus, especially sulfhydryl-containing drugs such as d-penicillamin (7
). On the basis of several reports of pemphigus occurring during pregnancy or with the use of oral contraceptives and disappearing thereafter, hormonal factors have been incriminated (8
, 9
). The potential role of sunlight had also been hypothesized, although the mechanism is unclear (4
). In Brazil, the epidemiologic features of pemphigus suggested an environmental cause (5
), and a case-control study found a significant association between pemphigus and frequent exposure to a black fly of the Simuliidae family (10
).
In Tunisia, as in other parts of the Arab world, series of cases suggest that pemphigus foliaceus is frequent among young women (11
, 12
). We conducted a comparative study of the epidemiology of pemphigus in France and Tunisia (13
). The study showed higher incidence rates of both pemphigus foliaceus and pemphigus vulgaris in Tunisia, explained mostly by a large number of cases in young women from rural areas. In these areas, the incidence rates were close to those of Brazil (20 new cases per million inhabitants per year). However, the absence of cases among children and the large predominance of young women contrasted with characteristics for Brazil. Thus, from both scientific and public health points of view, it is important to investigate the potential etiologic factors. Our hypothesis was that a large part of the excess incidence of pemphigus could be related to a risk factor more prevalent and/or more often expressed among young women living in rural areas. To test this hypothesis, we conducted a prospective case-control study in the female population of Tunisia. Risk factors studied were pregnancy, use of contraceptive pills, drugs, environmental factors (including those previously suspected in Brazil), and traditional Tunisian lifestyle (including cosmetic procedures).
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MATERIALS AND METHODS
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Study design
The study was conducted prospectively from May 1992 to February 1996. Because of the low incidence rate and the severity of this bullous disorder, a hospital-based case-control study involving all of the Tunisian departments of dermatology was used to estimate the potential risk factors. Cases and controls were matched for age (±5 years), hospital, date of hospital admission (within a 6-month period), and area of residence (urban vs. rural). Our goal was to recruit three controls per case. For a type I error of 5 percent, 55 cases were sufficient to detect, with a power of 80 percent, odds ratios greater than 2.5 for factors with a prevalence of 3050 percent in the general population and greater than five for factors with a prevalence of 5 percent. We recruited 73 incident female potential cases in a population of about 2 million adult women.
Cases
Cases were actively detected in all Tunisian dermatology departments (four in Tunis, one in Sousse, and one in Sfax). Potential cases were those hospitalized or referred to outpatient clinics with a diagnosis of recent pemphigus evolving for less than 1 year. Cases were validated and classified as pemphigus vulgaris or pemphigus foliaceus by an international group of dermatologists who reviewed photographs, pathologic slides, immunofluorescence studies, and standardized clinical information with the date of the onset of the disease, but who were not given the data on potential patients' exposure to risk factors. Antibodies against desmoglein 1 have not been used because the technique was not routinely available (14
).
Among the 73 potential incident cases, the review committee excluded three because of a delay between the onset of the disease and the interview of longer than 1 year. Relevant clinical information and direct immunofluorescence studies were available for all patients, photographs were available for 62 patients, pathologic data for 61, and indirect immunofluorescence studies for 33. The review committee excluded two cases because direct immunofluorescence was negative and indirect immunofluorescence was not available. Among the 68 remaining cases, according to the clinical pattern and the site of acantholysis on pathology, 38 (56 percent) were classified as pemphigus foliaceus, and 30 (44 percent) were classified as pemphigus vulgaris. The mean age at the onset of pemphigus was 37.9 years (13.5 standard deviation (SD)). The range was 2086 years.
Controls
Controls were female patients treated in the same hospital for an acute condition not suspected to be related to environmental factors and not related to a chronic disorder. We recruited controls among those who were referred to an outpatient clinic or were hospitalized for an acute condition, to avoid the potential repercussions of chronic illness on lifestyle and habits and the overrepresentation of patients with multiple chronic disorders. A list of potential acute conditions was defined a priori; those related to pregnancy or other gynecoobstetric conditions were not included. When three controls could not be obtained for a case, other controls were recruited among visitors of other patients. To avoid over- or underexposure to a particular factor, recruiters were advised to diversify the type of controls for each case. Diagnoses and delay from the first symptom were reviewed to determine the eligibility of the controls. Among the 170 controls who were interviewed, four were excluded because they did not fulfil the above mentioned criteria. The control group thus consisted of 166 patients. A total of 67 controls were admitted for infectious disorders, including urinary tract infection and pneumonia, 19 for abdominal emergency, 16 for trauma and acute osteoarticular pathology, and 16 for phlebitis or other conditions; 24 were outpatients with acute benign dermatologic disorders, and 24 were visitors. The prevalence rates of main exposures were analyzed in controls grouped as infectious disorders, emergency, visitors, and miscellaneous.
Data collection
Trained interviewers (H. T., I. M., R. N., and B. F.) performed the interviews of cases and paired controls. Because female patients could feel embarrassed about answering questions about personal habits, only women interviewers were recruited. A structured form was used to gather information on demographic characteristics, socioeconomic status, medical and gynecoobstetric history, drug intakes during the 6 months preceding the onset of the disease (or the date of interview for healthy controls), and environment. For information on drug use, patients were first read a list of symptoms and indications for potential treatment, followed by a list of drugs more frequently used by women and a list of sulfhydryl-containing drugs. For illiterate patients, boxes of these drugs were presented to cases and controls. Among environmental factors, we focused our attention on those associated with Brazilian pemphigus, living near a river and insect bites. We also investigated typical rural lifestyle, including working outdoors, farming, contact with animals, and home environment, including heating and cooking habits, traditional lifestyle, and cosmetic habits. The traditional Tunisian heating and cooking systems consist of a large clay bowl (called a kanoun), where people use charcoal, a small amount of oil, and sometimes wood, peat, etc. Cosmetic procedures currently used among Tunisian women include tfal, a clay used as peeling before Turkish baths; henna, a red- brown hair, nail, hand, or foot dye used as a dye; kohl, an antimony sulfide traditionally used as eyeliner; souak, a root of the walnut tree used to redden gum; and sugar-coated hair removal bands. Henna painting is gaining increasing popularity in Western countries, especially as a substitute for skin tattooing.
Statistical analysis
The data were analyzed with the use of standard case-control methods for the estimation of odds ratios and 95 percent confidence intervals (15
). The odds ratios were calculated separately for each exposure by using unconditional logistic regression models, forcing the matching variables into all models. The higher incidence rate of Tunisian pemphigus concerned both vulgaris and foliaceus forms; therefore, the odds ratios were not adjusted on the type of pemphigus.
Variables included in the final multivariate models were first selected using multiple two by two analyses, assessing interaction and confounding by fitting multiplicative models. These analyses were conducted with variables a priori associated with each other (e.g. different systems of home heating, different cosmetic habits, etc.) or variables that had significant relations among the control population. When an interaction was found or when the relation between variables was too important to separate the effect of each, a composite variable representative of the category was built. Then, a final backward step-by-step regression was conducted. The higher incidence rates were observed among young women (13
); this final model was then applied to the population of women aged 2035 years.
Data were analyzed using BMDP statistical software (University of California, Berkeley, Berkeley, California).
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RESULTS
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There was no significant difference between cases and controls for age, location of hospital, type of area (urban vs. rural), living conditions, education, and consanguinity (table 1).
No case and only one control had a history of autoimmune disease. Within the 6 months preceding the disease, few cases (7.4 percent) and controls (9.6 percent) used sulfhydryl-containing drugs, mainly bronchodilators. No patient reported d-penicillamine use. Within the year preceding the disease, 5 percent of the cases and controls used contraceptive pills. The total mean number of pregnancies (4.6 (2.6 SD) vs. 4.9 (2.9 SD)) and the occurrence of a pregnancy during the preceding year were similar in both groups (22.0 vs. 18.7 percent, p = 0.54).
Table 2 displays odds ratios for lifestyle and cosmetic habits. A significant greater proportion of cases than controls reported regularly frequenting Turkish baths and regular use of traditional tfal. A significant association was observed between these two variables. In joint analysis, no interaction was observed, and both variables remained significant; however, a decrease in the risk estimate of tfal use was observed (odds ratio (OR) = 1.4, 95 percent confidence interval (CI): 0.95, 2.9).
Most Tunisian women used henna as a hair dye or to paint their hands and feet; all of these habits were, however, more frequently reported by cases than by controls, with an OR of 7.3 (95 percent CI: 1.7, 31.9) when these habits were considered together. For each use (hair or nails, hands, and feet) and for all uses together, the estimates of the odds ratio increased with the frequency of use, suggesting a dose-dependent relation (table 3). When henna was used "sometimes," the estimate was 5.8, whereas when the use was reported "usually," the estimate was 12.1. Kohl appeared as a significant risk factor (OR = 3.9), with a modest dose-dependent relation. Cases reported using souak more often than did controls. No association was observed for other cosmetic procedures, such as facial make-up, traditional hair removal, and traditional tattoo. In bivariate analyses, independent roles of henna, kohl, and souak were observed, without statistically significant interaction. The different cosmetic habits were strongly associated in the control population (e.g., the use of souak was 10 times higher among controls who reported using henna than among those who did not). Considering the strength of the relations between use of cosmetics, a variable called traditional cosmetic was considered for multivariate models (none or one vs. two vs. three cosmetics (table 3)). Traditional cosmetic habits were associated with tfal use and frequentation of Turkish baths; in joint analysis, only cosmetics and frequentation of Turkish baths remained significant.
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TABLE 3. Odds ratio estimates for cosmetic habits according to the frequency of use in a multicenter case-control study, Tunisia, 19921996
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Table 4 displays risk estimates for potential environmental risk factors. No statistically significant association between pemphigus and living near a river or stagnant water was observed, nor was there an association with frequent fly bites. Cases more frequently reported wasp, bee, and spider stings than did controls; however, the exposures to insect stings were infrequent. Similar proportions of cases and controls reported farming activities, working outdoors, and regular contact with animals during a routine workday. However, more cases than controls reported daily care of ruminants and regular contact with cats and dogs. Similar proportions of cases and controls covered their arms and/or face during work outdoors.
The home heating system most frequently reported was traditional kanoun heating. A significant positive relation was observed for kanoun heating (OR = 3.0), and a negative relation (OR = 0.4) was seen for oil heating. There was a negative association between these two heating systems, without any significant interaction. In bivariate analyses, heating with oil was not associated with pemphigus. No relation between pemphigus and other heating systems was observed. Among cooking habits, cutting up raw poultry was strongly associated with pemphigus.
As shown in table 5, independent significant relations were observed between pemphigus and traditional cosmetics, regular frequentation of Turkish baths, cutting up raw poultry, contact with ruminants, and insect stings. All relative risks other than insect bites were higher when analysis was restricted to younger women (31 cases and 87 controls). We checked that there was not a statistically significant rejection of a good fit of the models (p = 0.6 and p = 0.9 for all women and for younger women, respectively). The prevalence rates of these exposures were similar across the categories of controls, except for visitors, who tended to have higher prevalence rates (table 6). However, results for the multivariate analysis excluding these 24 controls were similar to those of the entire group.
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TABLE 5. Multiple logistic regression model showing relations between traditional cosmetic habits, lifestyle, environmental exposures, and pemphigus, Tunisia, 19921996
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TABLE 6. Prevalence rates of main exposures among controls and a multiple logistic regression model excluding visitor controls, Tunisia, 19921996
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DISCUSSION
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To our knowledge, only one Brazilian study (10
), comparing 52 cases with 52 controls, has examined the risk factors for pemphigus. We did not observe an association between Tunisian pemphigus and the risk factors identified in Brazil (fly bites and living near a river) or suspected in Europe and North America, such as sulfhydryl-containing drugs, autoimmune disorders, pregnancy, and contraceptive pills. Conversely, we have observed a significant association between pemphigus and the traditional Tunisian lifestyle, e.g., contact with ruminants, cutting up raw poultry, Turkish baths, and cosmetics. Odds ratios were substantial; moreover, when analysis was restricted to the population of young women, in whom pemphigus is highly prevalent, most odds ratios increased.
The validity of this study depends on many factors, including the unbiased recruitment of cases and controls and the accuracy of the information obtained about potential exposure. This study was designed to include all cases admitted to one of the six Tunisian departments of dermatology. Because pemphigus is a severe bullous disorder, we postulated that nearly all cases are referred to the hospital. As in all hospital-based case-control studies, selection bias cannot be totally excluded, but we do not suspect any direct relation between selection of patients and exposures. The number of cases recruited is compatible with the incidence rate previously observed (13
). Hospital controls were chosen for logistic reasons. To limit bias, controls were selected among subjects hospitalized for an acute disease a priori unrelated to the potential risk factors (16
). Additionally, the diversity of diseases among controls makes it unlikely that any particular exposure was over- or underrepresented. Except for visitors, little difference between groups of controls was found for significant exposures, and the multivariate analysis excluding these visitors provided results close to those observed for the entire group. Analyses comparing cases with each category of controls evidenced some fluctuations of odds ratios related to the small numbers, but the odds ratios were generally consistent (data not shown). Similarities between cases and controls in terms of place of residence, type of area, living conditions, and educational attainment were fairly good. This study was designed to assess potential environmental exposures, drugs, and hormonal factors. Because neither patients nor physicians usually consider Tunisian pemphigus to be induced by specific environmental factors, we do not think that our study suffered from recall bias. Furthermore, memory about lifestyle may be less biased by patient (case or control) status than the memory of a precise event (17
).
Finally, major confounders were taken into account by matching factors and by adjustment during analyses. Since the incidence rate of pemphigus was higher in rural areas among women living in poor conditions (13
), matching on area and adjustment was important to identify specific risk factors.
We found strong associations between pemphigus and several environmental factors. With regard to insect bites, our study does not substantiate the hypothesis of a role of fly bites in pemphigus among Tunisian women. The role of the Brazilian blackfly, which was confirmed by a case-control study (10
), was previously suspected because of a series of cases that demonstrated that pemphigus cases lived near rivers, which are breeding areas for Simulium flies, and because incident cases increased during the period of insect multiplication (5
). No such phenomenon was previously reported in North Africa. In Tunisia, the unexpected association between pemphigus and wasp, bee, and/or spider stings concerns only occasional exposure. Since these bites are the most spectacular ones and cases who experienced severe cutaneous lesions were more prone to remember other cutaneous lesions, bias should be considered (18
). We cannot exclude the possibility that initial lesions of pemphigus were interpreted by the patients as insect bites.
We observed an association between pemphigus and daily care of ruminants. This has not been reported previously; however, this relation has not been specifically studied even though patients with Brazilian pemphigus were usually peasants (6
, 10
). The similar proportions of cases and controls who reported farming activities, working outdoors, and having regular contact with animals do not support the hypothesis of a selection bias. The credibility of the association is reinforced by the strength of the association and the higher point estimate among the population of younger women. Similar results were observed for cutting up raw poultry, with an increase of the point estimate from 5.1 to 11.4. These two findings suggest the possibility of a transmissible agent.
Regular frequentation of Turkish baths is common in Tunisia, but the number was much higher among cases, and the odds ratio was twice as high among younger women. Use of traditional cosmetics (kohl, henna, and souak) was a strong risk factor for pemphigus, while no association was observed for commercial cosmetics. The strong links between these habits could suggest that this association merely reflects lifestyle rather than a direct effect of cosmetics. Nevertheless, the strength of the association, the increase in the odds ratios among women aged 2035 years, and the relation between dose and effect suggest a causal association. Tunisian women commonly use traditional cosmetics after marriage for daily care and for social occasions. Kohl is believed to consist of antimony, but several studies analyzing samples from different countries indicated the presence of other elements such as lead, aluminum, carbon, iron, titanium, silver, silicon, and trace amounts of antimony (19
, 20
). Some kohl with a high level of lead was responsible for childhood lead poisoning (21
). To obtain henna dye, dry leaves of Lawsonia inermis are mixed with oil and various substances such as charcoal powder, lampblack, or "secret formulas" that may contain p-phenylenediamine. Reactions to henna such as urticaria, angioedema, and contact dermatitis have been reported occasionally (22
24
), suggesting that it can be allergenic. We had postulated that the excess number of pemphigus cases in Tunisia was probably related to some factor(s) more prevalent or more often seen among young women. This factor could be traditional cosmetics that are commonly and specifically used by women in all of North Africa. The very high prevalence of use compared with the relatively low incidence rate of pemphigus substantiates the hypothesis of an interaction between individual susceptibility and risk factors. In the other form of endemic pemphigus observed in Brazil, an interaction has recently been demonstrated between antibodies against desmoglein and the risk of pemphigus; the disease is triggered by chronic skin aggression by Simuliidae (14
). In Tunisia, the pathogenic autoantibody response in a predisposed person may be triggered and maintained by chronic antigenic stimulation associated with cosmetic use. In berylliosis, an interaction between chemical exposure and genetic factors has been demonstrated (25
). Such an interaction should be searched for in Tunisian pemphigus.
Thus, our study evidenced several factors that are strongly associated with pemphigus. The fact that cosmetics are used only by women strongly suggests the potential causative role of these factors. However, considering the strong associations of these factors altogether, even though each factor remained significant in multivariate analysis, further studies are necessary to demonstrate that these factors are not simply markers identifying a population exposed to another factor, which could explain the excess of cases of pemphigus.
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ACKNOWLEDGMENTS
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Supported by a grant from INSERM (contract 491NS5).
The authors are indebted to Professor Jean Revuz for his participation on the review committee, to Anne Puel for her assistance in data management, and to Professor Isabelle Durand-Zaleski for her helpful review of the paper.
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NOTES
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Reprint requests to Dr. Sylvie Bastuji-Garin, Service de Santé Publique, hôpital Henri-Mondor, 51, av, du Mal de Lattre de Tassigny, 94010 Créteil, Cedex, France (sylvie.bastuji-garin{at}hmn.ap-hop-paris.fr).
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REFERENCES
|
---|
-
Stanley JR. Cell adhesion molecules as targets of autoantibodies in pemphigus and pemphigoid, bullous diseases due to defective epidermal cell adhesion. Adv Immunol 1993;53:291325.[ISI][Medline]
-
Hietanen J, Salo OP. Pemphigus: an epidemiological study of patients treated in Finnish hospitals between 1969 and 1978. Acta Dermatovenereol 1982;62:4916.[ISI][Medline]
-
Korman N. Pemphigus. J Am Acad Dermatol 1988;18:121938.[ISI][Medline]
-
Bastuji-Garin S. Acquired autoimmune bullous skin disease. In: Grob JJ, Stern RS, MacKie RM, et al., eds. Epidemiology, causes and prevention of skin diseases. Oxford, England: Blackwell Science, Ltd, 1997:33441.
-
Diaz LA, Sampaio SA, Riviti EA, et al. Endemic pemphigus foliaceus (fogo selvagem). II. Current and historic epidemiologic studies. J Invest Dermatol 1989;92:412.[Abstract]
-
Empinoti JC, Diaz LA, Martins CR, et al. Endemic pemphigus foliaceus in Western Parana, Brazil (19761988). Br J Med 1990;123:4317.
-
Mutasim DF, Pelc NJ, Anhalt GJ. Drug-induced pemphigus. Dermatol Clin 1993;11:46371.
-
Goldberg NS, DeFeo C, Kirshenbaum N. Pemphigus vulgaris and pregnancy: risk factors and recommendations. J Am Acad Dermatol 1993;28:8779.[ISI][Medline]
-
Honeyman JF, Eguiguren G, Pinto A, et al. Bullous dermatoses of pregnancy. Arch Dermatol 1981;117:2647.[Abstract]
-
Lombardi C, Borges PC, Chaul A, et al. Environmental risk factors in endemic pemphigus foliaceus (fogo selvagem). J Invest Dermatol 1992;98:84750.[Abstract]
-
Morini JP, Jomaa B, Gorgi Y, et al. Pemphigus foliaceus in young women. An endemic focus in the Sousse area of Tunisia. Arch Dermatol 1993;129:6973.[Abstract]
-
Haouet H, Ben Amida A, Haouet S, et al. Le pemphigus tunisien. A propos de 70 cas. (Expérience du service de dermatologie de l'hôpital La Rabta, de 1974 à 1992). Ann Dermatol Venereol 1996;123:911.[ISI][Medline]
-
Bastuji-Garin S, Souissi R, Blum L, et al. Comparative epidemiology of pemphigus in Tunisia and France: unusual incidence of pemphigus foliaceus in young Tunisian women. J Invest Dermatol 1995;104:3025.[Abstract]
-
Warren SJP, Lin MS, Giudice GJ, et al. The prevalence of antibodies against desmoglein 1 in endemic pemphigus foliaceus in Brazil. N Engl J Med 2000;343:2330.[Abstract/Free Full Text]
-
Breslow NE, Day NE, eds. Statistical methods in cancer research. Vol I. The analysis of case-control studies. Lyon, France: International Agency for Research on Cancer, 1980. (IARC scientific publication no. 32.).
-
Wacholder S, Silverman DT, McLaughlin JK, et al. Selection of controls in case-control studies. II. Types of controls. Am J Epidemiol 1992;135:102941.[Abstract]
-
Raphael K. Recall bias: a proposal for assessment and control. Int J Epidemiol 1987;16:16770.[ISI][Medline]
-
Sackett DL. Bias in analytic research. J Chronic Dis 1979;32:5163.[ISI][Medline]
-
al-Hazzaa SA, Krahn PM. Kohl: a hazardous eyeliner. Int Ophthalmol 1995;19:838.[ISI][Medline]
-
Parry C, Eaton J. Kohl: a lead-hazardous eye makeup from the Third World to the First World. Environ Health Perspect 1991;94:1213.[ISI][Medline]
-
Mojdehi GM, Gutner J. Childhood lead poisoning through kohl. Am J Public Health 1996;86:5878.[ISI][Medline]
-
Lestringant GG, Bener A, Frossard PM. Cutaneous reactions to henna and associated additives. Br J Med 1999;141:598600.
-
Majoie IN, Bruynzeel DP. Occupational immediate-type hypersensitivity to henna in a hairdresser. Am J Contact Dermat 1996;7:3840.[Medline]
-
Etienne A, Piletta P, Hauser C, et al. Ectopic contact dermatitis from henna. Contact Dermatitis 1997;37:183.
-
Richeldi L, Sorrentino R, Saltini C. HLA-DPB1 Glutamate 69: a genetic marker of beryllium disease. Science 1993;262:2424.[ISI][Medline]
Received for publication September 14, 2000.
Accepted for publication September 4, 2001.