Natural rubber latex allergy in the occupational setting

Natural rubber latex allergy in the occupational setting

Methods 27 (2002) 15–21 www.academicpress.com Natural rubber latex allergy in the occupational setting B. Lauren Charous,a,* S.M. Tarlo,b M.A. Charou...

91KB Sizes 0 Downloads 79 Views

Methods 27 (2002) 15–21 www.academicpress.com

Natural rubber latex allergy in the occupational setting B. Lauren Charous,a,* S.M. Tarlo,b M.A. Charous,c,d and K. Kellyd a

Milwaukee Medical Clinic, Allergy and Respiratory Care Center, Advanced Healthcare, SC, 3003 West Good Hope Road, Milwaukee, WI 53209, USA b University of Toronto, Toronto, Canada c Health Psychology Associates, Milwaukee, WI, USA d Medical College of Wisconsin, Milwaukee, WI, USA Accepted 18 March 2002

Abstract Over the last decade, the prevalence of natural rubber latex (NRL) allergy has reached epidemic proportions among workers who use or who are exposed to powdered latex products. NRL-associated occupational asthma is confined largely to those exposed to powdered latex glove use or other latex aerosols. The most frequent presenting symptom of NRL allergy is contact urticaria; inhalation may cause symptoms of allergic rhinitis and asthma. Skin prick testing is the most accurate tool for diagnosis of NRL allergy. The cornerstone of management is cessation of exposure; substitution with non-NRL or nonpowdered NRL gloves results in predictable rapid disappearance of latex aeroallergen. Ó 2002 Elsevier Science (USA). All rights reserved. Keywords: Natural rubber latex; Allergic sensitization; Latex gloves; Latex allergy; Occupational asthma; Occupational allergy; Anxiety disorder; Standard precautions

1. Introduction Natural rubber latex (NRL), commonly referred to as ‘‘latex,’’ has been widely used in medical devices for more than a century owing to an attractive combination of properties: strength, flexibility, tear resistance, elasticity, and barrier qualities. Latex gloves were developed by the latter half of the 19th century due to the ease of manufacturing dipped latex products and the superior tactile qualities of the resultant product. The advent of ‘‘universal precautions’’ in the 1980s expanded the use of nonsterile (exam) NRL gloves—more than 20 billion pairs were sold in the United States alone in 1999 [1]. During most of the last century the only problem encountered with NRL glove use was the increased prevalence of contact dermatitis. This was due either to an allergic contact dermatitis sensitivity to a chemical additive used in NRL manufacture or to a nonspecific irritation associated with glove use rather than a hy-

*

Corresponding author. E-mail address: [email protected] (B.L. Charous).

persensitivity response to the NRL proteins. Hence, reports of anaphylactic reactions to NRL products, including some fatalities, that appeared little more than a decade ago were unanticipated. Three distinct groups at high risk were initially identified: children with spina bifida; patients who had undergone radiological examinations that used latex rubber barium enema retention balloons; and individuals using NRL gloves frequently at work, especially health care workers. Later it became apparent that the risk included other individuals who underwent frequent surgical procedures and those with other occupational exposures to NRL. Fortunately, many such nonoccupational reactions have been prevented by institution of prophylactic safety measures such as avoidance of NRL products from birth in children with spina bifida/congenital urological abnormalities and removal of NRL from radiological catheter tips. Reports of allergic reactions in health care workers began appearing in the early 1990s and generated an ongoing discussion regarding the risk of occupational disease associated with chronic exposure to latex products [2]. What is the nature of the risk of sensitization to latex among health care workers and others who wear

1046-2023/02/$ - see front matter Ó 2002 Elsevier Science (USA). All rights reserved. PII: S 1 0 4 6 - 2 0 2 3 ( 0 2 ) 0 0 0 4 7 - 6

16

B.L. Charous et al. / Methods 27 (2002) 15–21

latex gloves? Is this sensitization clinically relevant? Do clinical symptoms of contact hives, rhinoconjunctivitis (‘‘hay fever’’), asthma, and anaphylaxis occur more frequently than in nonexposed individuals? Which latex products are responsible for causing symptoms? Most importantly, since the diagnosis of occupational allergy and asthma implies significant human, legal, and economic costs, how and at what cost can a safe workplace be established? Many of the answers to these questions have become available through international efforts. Studies from several groups working independently demonstrate remarkably consistent findings concerning the occupational nature of this problem [3–5]. 2. Risk factors for allergic sensitization Atopic individuals are predisposed to sensitization and clinical allergy as compared with nonatopic individuals—a generalization as true for latex as for other allergens. Nonetheless, the chief risk factor for latex allergy is clearly related to exposure. Population prevalence studies that use skin prick testing, the most accurate assessment tool, report positive tests in 5–12% of NRL-exposed workers [6–8]. Nearly half of these sensitized health care workers report a history of allergic reactions. In one study, 50% of allergic workers with no history of asthma experienced an asthmatic response during a ‘‘glove handling’’ inhalation challenge [9]. This finding suggests that chronic exposure to latex aerosol in NRL-allergic individuals carries the risk of provoking lower airway inflammatory responses and asthma. Observed rates of 2–10% occupational asthma (OA) in chronically exposed workers justify these concerns [8,10,11]. In contrast, only 2–3% of nonexposed atopic individuals and only 1% of the general population demonstrate positive skin tests to NRL. More importantly, allergic symptoms related to NRL exposure are rarely reported in these groups [3,6,12]. Delineating the relationship of latex sensitization and allergy to the duration and extent of latex exposure has been the object of recent research. Three studies investigated the effect of increased latex exposure on those entering the workplace and are especially relevant to an understanding of the epidemiology of occupational disease, since they avoid the problems of only healthy individuals remaining in the study population (survivor bias). Tarlo et al. [13] reviewed cross-sectional rates of latex sensitization and allergy in University of Toronto Dental School students and faculty. None of the firstand second-year dental students tested were allergic. In contrast, 5% of third-year and 10% of the fourth-year students had become sensitized. One-quarter of tested faculty had positive skin tests to natural rubber latex and 9% of faculty who completed the questionnaire reported asthma symptoms on exposure to latex gloves.

Levy et al. [14] performed a similar study on dental students in London and Paris. None of 86 preclinical students had a positive skin test. In contrast, of the 189 graduating students, 11 (6%) were latex allergic. A prospective study completed by the University of Montreal group studied the incidence of occupational allergy and asthma in more than 750 apprentice workers in three diverse categories: in animal health, in pastry making, and in dental hygiene [15,16]. On entry, the prevalence of latex allergy was insignificant in all three groups. However, during the course of the study striking differences emerged. Only in the dental hygiene apprentices, who used latex gloves regularly, did latex allergy become more widespread. The cumulative incidence for skin sensitization was 6.4% and that for OA was 4.5% over the 32 months of observation. Underlining the potency of latex as an aeroallergen, the authors observed the likelihood of latex sensitization in a dental hygiene apprentice was greater than the likelihood of animal-derived allergen sensitization in an animal health apprentice over a similar period. Evidence suggests that sensitization to latex, as with other allergens, is influenced not only by the duration but also by the amount of exposure. In the dental student study previously cited, Levy et al. [14] noted that latex allergy was not evenly distributed among the dental students, but rather was confined to those who had used powdered latex gloves. In fact, none of the 93 graduating dental students who had used only powder-free proteinpoor gloves was latex allergic. Similarly, in a follow-up study at the University of Toronto School of Dentistry, a change to low-protein, powder-free NRL gloves resulted in complete absence of skin test responses to NRL extract among those assessed in subsequent student classes [17]. Baur et al. [18] also reported analogous findings in a study of aeroallergen exposure. They screened 145 subjects and performed aeroallergen sampling in 32 hospital and operating rooms and physicians’, offices. Latex aeroallergen concentrations varied widely, ranging from undetectable levels to 205 ng=m3 . Fifteen percent of the workers showed evidence of latex allergy; however, all of the individuals who were sensitized had worked in areas where aerosol concentrations were at least 0:6 ng=m3 . This observation suggests that like other industrial allergens, a threshold for latex aeroallergen may exist that is associated with the generation of sensitization and subsequent symptoms.

3. Sources and routes of exposure Most patients allergic to latex have significant exposure to rubber products made by a dipping method. While only a minority of latex products are made by this method, most allergic reactions to latex are associated with products of this type, such as latex medical gloves,

B.L. Charous et al. / Methods 27 (2002) 15–21

condoms, bladder catheters, and tourniquets. The manufacture of these items uses a lower temperature and a shorter duration of heat vulcanization when compared with latex products made from coagulated or dry rubber. This appears to be the cause of the observed higher allergen content in the finished rubber product. Latex exposure can take place either through direct skin/mucous membrane contact or via inhalation. The first route of exposure may sensitize those who wear latex gloves regularly, especially individuals with contact dermatitis in whom the normal barrier function of the skin is disturbed [13]. Typically, initial symptom of latex allergy in this group is a contact reaction such as urticaria or acute erythema with pruritis that occurs on skin directly exposed to NRL gloves. However, such symptoms may be relatively mild and may be ignored by the worker, who may subsequently present with anaphylaxis due to mucous membrane exposure to NRL after blowing up balloons or during a personal dental/medical surgical visit. Respiratory symptoms of allergic rhinitis, conjuctivitis, and asthma due to NRL allergy can occur as part of a systemic anaphylactic response but more frequently occur due to inhalation of aerosolized NRL. Numerous studies have found appreciable levels of aeroallergen in medical settings, with concentrations ranging from less than 1 to more than 300 ng=m3 . It is worth noting that these airborne concentrations are similar in magnitude to the concentrations of several other aeroallergens, including laboratory and domestic animal proteins, flour dust, and papain, which are known to induce OA [19]. Dipped latex products, such as latex gloves, that are powdered postvulcanization are particularly problematic because of the ability of the powder to function as a carrier of latex proteins, resulting in airborne exposure [20,21]. In the medical setting, the generation of latex aeroallergen has been shown to be dependent on the active use of powdered latex gloves [22–24]. When nonpowdered latex or nonlatex gloves are substituted for powdered latex gloves, latex aeroallergen levels predictably disappear, even when no other preventative measures are taken. This decline in latex aerosol levels takes place rapidly. During evening or other nonworking hours, latex aerosol can become undetectable in rooms without carpeting or other long-term repositories [22,25]. Continued use of powdered latex gloves, moreover, exposes not just the wearer to latex aerosol, but coworkers and patients as well. In an investigation into the sources and dispersion of latex aeroallergen in a multipractitioner dental office [25], aeroallergen sampling confirmed the dispersion of latex aerosol into work areas where only nonpowdered latex or nonlatex gloves were used from other areas where powdered latex gloves were still in use. Measurable concentrations of latex aerosol were also observed in the patient waiting area ð7 ng=m3 Þ and in all the other opertories, hygiene rooms, and laboratories sampled (14–90 ng=m3 ). An initial at-

17

tempt to substitute nonpowdered latex gloves throughout the office was not effective in eliminating latex aeroallergen in the office. This failure was explained by the discovery of continued but unannounced use of powdered gloves in one opertory. Introduction of ‘‘lightly powdered’’ lower allergen gloves in that area led to the disappearance of latex aerosol from all offices except the rooms where such powdered gloves continued to be used. These observations strongly suggest that implementation of appropriate glove procurement policies may eliminate latex aerosol and prevent both sensitization of glove wearers and inadvertent secondary exposure of latex-allergic patients. Further support for such an approach comes from an evaluation of annual identified cases of NRL allergy among health care workers in Ontario’s largest hospital [26]. In this study the annual number of cases rose until 1995 when a change was made to powder-free, lowprotein NRL gloves. Subsequently, the number of cases as reflected by hospital incidence reports and allergy clinic visits rapidly fell. Similar temporal changes were seen in accepted claims for occupational asthma due to NRL allergy in Ontario, concurrent with glove changes in several Ontario hospitals [27].

4. Presentations and diagnosis of latex allergy The diagnosis of contact dermatitis should be considered for patients who describe skin rashes that persist beyond several hours or that are chronic. In our experience, most of these patients have a nonspecific irritant dermatitis. However, cases of allergic contact sensitivity to rubber accelerators, such as thiuram, are not infrequent, and patch testing can provide a definitive diagnosis. Physicians should be aware that contact dermatitis and type I latex allergy are not mutually exclusive diagnoses. Acute contact urticaria or a pruritic erythematous rash occurring within 30–60 min of donning gloves is strongly suggestive of a possible type I reaction, mediated by anti-latex IgE. There is a broad spectrum of respiratory complaints attributable to latex allergy. Some patients connect worsening symptoms with on-the-job exposure. However, sneezing, ocular tearing, and itching, severe rhinorrhea, and nasal stuffiness may be indistinguishable from acute seasonal pollenosis. In those cases where the patient is unaware that latex is causing or is contributing to discomfort, the possibility of latex allergy may be suggested by positive responses appearing on a screening questionnaire. Latex occupational asthma may present as a classic syndrome of wheezing and shortness of breath occurring or worsening at work. However, the course of worsening asthma may be so gradual that it may be missed or may not be recognized as due to workplace exposure. Even

18

B.L. Charous et al. / Methods 27 (2002) 15–21

patients with a history of other acute on-the-job symptoms, such as contact urticaria, cannot always identify the source of their asthma. The existence of other concurrent exposures, both occupational and nonoccupational, such as to domestic pets or to house dust mites, may further confuse the picture. Therefore, all asthmatics with latex allergy who have potential exposure to airborne latex in their workplace should be investigated for possible occupational asthma. Occupational latex allergy may be diagnosed using medical history, physical examination, laboratory testing, patient testing, workplace analysis, and response to avoidance of latex. The medical history should include an exposure history, symptom onset, effect of vacation or time away from work on symptoms, atopic history, prior history of surgery, asthma, and allergic reactions during surgery and progression of symptoms. There are a number of unique features of the medical history in a patient with latex allergy that require highlighting. A complete review of the medical history is most critical prior to a medical or dental procedure where contact of mucosal surfaces with latex is anticipated. Many individuals who develop occupationally related latex allergy describe antecedent dermatitis, either irritant or allergic contact dermatitis, originating at the site of direct exposure (e.g., on the hand). In addition to common allergic symptoms of contact urticaria, rhinoconjunctivitis, or asthma, some latex-allergic individuals describe a history of oral allergy or systemic symptoms after ingestion of banana, kiwi, avocado, chestnut, stoned fruits, as well as other cross-reactive foods. The most reliable and sensitive test for latex allergy is a skin prick test that employs a test allergen containing relevant antigenic epitopes. Several commercial preparations have been released in Europe and Canada that appear to be highly specific and sensitive [28–30]. In the United States, confirmatory diagnosis by means of skin prick testing continues to be hindered by the lack a standard skin test reagent. Allergists have commonly employed fresh extracts of products or foods (e.g., banana) because of their superior sensitivity as compared with commercial extracts. In contrast, however, use of NRL test extracts derived from ‘‘causative’’ latex-containing medical devices or products of unknown potency has caused significant problems. These extracts appear to be much more variable in potency and, accordingly, their use has been compromised both by observed problems with inadequate sensitivity (leading to a falsenegative result) and by the provocation of systemic symptoms [31]. A nonammoniated extract of latex (NAL) has been shown to be highly sensitive and specific in a particular population with a high prevalence of latex [32]. The clearance of NAL skin testing reagent by the US FDA is in process. Alternatively, use of serologic assays for detection of anti-latex IgE may be used. The Pharmacia’s CAP,

Diagnostic Product AlaSat, and Hycor’s Hytech are available. In cohorts of populations studied where the prevalence of disease is high, the sensitivity of the assays may be greater than 95%. More problematic is use of these tests in screening populations with a low prevalence ð< 1%Þ of latex allergy. Bayesian statistical analysis predicts that > 90% of these assays will yield false positives when applied to populations with low prevalence of disease. In a like manner, this explains the observation that 6% of blood bank samples may yield a positive test (see [33] for a more complete discussion of this problem). Thus, in the United States, physicians are still faced with using clinical judgment in a symptomatic patient. The use of direct challenge tests with either a glove ‘‘use’’ test or modified use test with pricking of the skin may be helpful. However, this technique suffers from the same sensitivity issues of ‘‘homemade’’ latex extracts including false-negative and potential systemic reactions. This testing has most commonly been done with the offending products, most often a powdered latex glove. Initially a single digit of the glove is donned for 20 min. Evaluation of pruritis, erythema, hives, or other allergic symptoms is performed. If no reaction ensues, the hand is moistened and the latex glove is placed on the hand. A control vinyl glove may be used on the other hand. A 1-mm lancet may be used to prick the back of the hand in three spots either prior to donning the glove or through the glove. The pursuant risks, benefits, and false-negative responses limit the value of this approach. Even when the diagnosis of latex allergy is confirmed by any of these methods, clinicians should exercise caution before concluding that complaints such as cough, shortness of breath, and chest tightness are due to latex-induced occupational asthma. As is the case with other occupational exposures, confirming the relationship between asthmatic symptoms/signs and latex exposure may be challenging. A recent report underlined the poor predictive value of combined clinical history and immunologic tests alone for the purpose of confirming a suspected diagnosis of OA [34]. Specific inhalation challenge is the most reliable diagnostic test, but this test is also time consuming and expensive and currently available at only a few research centers. In its place, workplace monitoring (pre-, during, and postshift peak expiratory flow rates or spirometry) has been used, although lack of patient compliance and effort can compromise this approach. Serial methacholine challenges, performed at the end of a work week and after a few weeks off work, can be used with this to provide more objective documentation of changes in airway responsiveness related to work. In cases of severe asthma, employees should be removed from the workplace and challenges or serial monitoring should be postponed until the patient is stabilized.

B.L. Charous et al. / Methods 27 (2002) 15–21

5. Psychological aspects In some patients, presumed or real latex allergy may pose psychological diagnostic challenges for the clinician. Consideration of an anxiety disorder should be included in the differential diagnosis for those patients who exhibit symptoms of pervasive or acute sensations of shortness of breadth, chest tightness, and difficulty breathing that do not appear to be satisfactorily explained by the severity of their latex-induced asthma. It is worth emphasizing that many of these patients do have both significant histories of occupational exposure and objective evidence of latex allergy and/or asthma. It has been appreciated for some time that asthma and other respiratory disorders provoke a high level of anxiety [35–41]. This problem may be accentuated in latex-allergic workers who have already experienced severe reactions or anaphylaxis. Simple avoidance measures used for other potent discretely encountered allergens (e.g., stinging insect venoms or pencillin) may be viewed as providing precarious safety given the ubiquity of latex in the medical setting. In addition, the tendency of latex to provoke reactions ‘‘by proxy’’ in patients sensitive to a wide range of cross-reactive foods can further create a sense of unease in affected patients. The consequent sensation of being ‘‘always at risk’’ [42] may engender anticipatory reactions in some patients and/or a state of hypervigilance and increased autonomic reactivity characteristic of anxiety reactions, commonly known as the ‘‘fight or flight’’ response. Thus, a fear/panic reaction may occur due to the presence of perceived stimuli or even in the apprehension of the unknown. Furthermore, in individuals with airway hyperreactivity, panic-induced hyperventilation may actually provoke bronchospasm and further intensify symptoms of chest tightness and shortness of breath [40]. While it may be tempting either to suspect malingering or to dismiss or discount problematic symptomatic patients, malingering is a fairly uncommon diagnosis in individuals who have a stable work history, professional accomplishments, a prior stable psychological adjustment, and a balanced life situation. It appears more likely that many of these individuals may be experiencing either conditioned fear reactions [43–45], behavioral sensitization [46], or behavioral responses acquired through social contagion. Additionally, changes in airway tone may also be mediated by psychological stimuli [47]. Previous ‘‘bona fide’’ acute reactions including anaphylaxis experienced by these individuals may trigger subsequent anxiety attacks, possibly intensifying feelings of panic. Increased autonomic reactivity experienced by some of these patients may result in symptoms that ‘‘mimic latex allergy’’ [48].

19

Like other patients with chronic illnesses, psychological distress secondary to coping with the strain of and adjustment to living with health problems may find expression in emotional responses such as denial, anger, depression, anxiety, grief reactions, and strained relationships with family and friends. When individuals are unable to maintain their current profession, the loss of occupational status may result not only in serious financial distress due to loss of future earnings or forced early retirement, but may also have significant effects on self–esteem and the achievement of life goals. Many of the affected patients are health care professionals whose primary identification is with their job—‘‘I’m an ICU nurse.’’ For them, the diagnosis of latex allergy can mean ‘‘the loss of life as you know it.’’ Latex allergy, like all other chronic illnesses, can also have profound effects on family functioning. Additional family responsibilities may create ‘‘caregiver stress’’ in the patient’s spouse, and young children may internalize the fear reactions of the latex allergic parent. Depression, anxiety, and quality of life decrements should be assessed for the newly diagnosed latex patient and should be monitored if the patient’s disease continues to progress. The patient needs to be provided with education at the time of diagnosis and reassurance that with the necessary precautions he or she can continue to maintain much of the normalcy prior to their latex diagnosis. Patients who exhibit adjustment difficulties should be referred for adjunctive psychological treatment where they can learn active coping skills such as stress management, relaxation therapy, breathing retraining, and cognitive–behavioral treatment. Early intervention and multidisciplinary collaboration can reverse the potential for the initiation of a negative trajectory of psychological adjustment in individuals with comorbid stress and anxiety reactions.

6. Management of NRL-allergic patients The cornerstone of successful management of occupational latex allergy and asthma rests on the institution of cessation of exposure. Powdered latex gloves are the major and perhaps only significant source of workplace latex aeroallergen. Prior to the introduction of ‘‘standard precautions’’ for protection against communicable disease from blood and bodily fluids, protective devices such as gloves were used only in selected settings. The almost 10-fold increase in examination glove (not surgical or sterile gloves) use in the United States can be linked to this policy. This increase in glove use, coupled with failures to set a standard for maximal amount of releasable latex allergen from gloves and failure to recognize the role of cornstarch donning powder as a respiratory source of allergen, is largely responsible for the

20

B.L. Charous et al. / Methods 27 (2002) 15–21

epidemic of occupational respiratory allergic responses to latex. There are enough clinical data today to outline a commonsense, effective strategy for prevention of latex allergy while continuing to use safe effective barriers to infectious disease transmission. First, all subjects who do not contact contaminated bodily fluids should use a nonlatex material (e.g., food handlers). Although latex is a superb barrier, newer synthetics (e.g., nitrile) offer clinically effective and functionally indistinguishable alternatives. To our knowledge, despite multiple in vitro tests favoring the barrier of latex, no clinical practice studies demonstrate any increase in risk of infectious diseases being acquired by humans from the use of nonlatex gloves that have been approved for distribution and meet barrier standards set by US FDA. Second, when nonsterile (i.e., examination) latex gloves are used, only nonpowdered gloves should be used. Because the cost of conversion in examination glove use is not appreciable, nonpowdered latex gloves have already surpassed sales of powdered latex gloves. Sterile latex gloves appear as only an uncommon cause of problems in nonsensitized individuals. For this reason, use of lowprotein powdered (< 50 lg=gm ASTM D5712) surgical sterile gloves is acceptable if accompanied by an ongoing monitoring program for latex allergy [49]. Those institutions that wish to successfully return a latex-allergic worker to her or his job must adhere to policies that allow use of only low-allergen, powder-free latex gloves by the other workers so that continued exposure is eliminated. Because subjects who wear powdered latex gloves may move throughout an institution and air handling systems may recirculate aeroallergen [25], it is critical that these standards be applied throughout a building. It should be viewed as no longer acceptable for a worker to have a ‘‘special’’ glove that he or she likes if it endangers the health of others. Workers who report contact or allergic rhinoconjunctivitis symptoms at work and have confirmatory skin tests for latex allergy not only must avoid latex gloves themselves, but also must avoid proximity to coworkers who use powdered latex gloves. The use of  blockers by such patients is contraindicated since it may block therapeutic response to drugs used for treatment of anaphylaxis. Patients with chronic rhinoconjunctivitis may benefit from intermittent topical nasal steroids. On the other hand, routine use of antihistamines may mask the onset acute symptoms of exposure and result in a more prolonged, and possibly more severe, reaction. Treatment of occupational asthma also often requires use of inhaled corticosteroids, at times at high doses or supplemented with an initial burst of oral corticosteroids. Addition of other antiasthmatic agents, including long-acting bronchodilators, leukotriene receptor antagonists, and theophylline, may be helpful. Other fac-

tors contributing to asthma, such as gastroesophageal reflux, vocal cord dysfunction, and other allergic exposures, should be assiduously sought and treated. Similar to other types of OA, despite aggressive treatment and cessation of exposure, asthma may persist months or years after removal from the job.

References [1] US Food and Drug Administration (US FDA) Fed. Regist. 64 (1994) 41710–41743. [2] B.L. Charous, R.G. Hamilton, J.W. Yunginger, J. Allergy Clin. Immunol. 94 (1994) 12–18. [3] K. Turjanmaa, S. M€akinen-Kiljunen, T. Reunala, H. Alenium, T. Palosuo (Eds.), Natural Rubber Latex Allergy: The European Experience, Saunders, Philadelphia, 1995. [4] O. Vandenplas, B. Charous, S. Tarlo, Latex Allergy, in: I. Bernstein, M. Chan-Yeung, J.-L. Malo, D. Bernstein (Eds.), Asthma in the Workplace, Second ed., Marcel Dekker, New York, 1999, pp. 425–444. [5] J. Taylor, P. Wattanakri, B. Charous, D. Ownby, in: B. Theirs, P. Lang Jr. (Eds.), 2000 Year Book of Dermatology and Dermatologic Surgery, Mosby, St. Louis, 1999, pp. 325–368. [6] R. Arellano, J. Bradley, G. Sussman, Anesthiology 77 (1992) 905– 908. [7] G. Liss, G. Sussman, K. Deal, S. Brown, M. Cividino, S. Siu, et al., Occup. Environ. Med. 54 (1997) 335–342. [8] O. Vandenplas, J.-P. Delwiche, G. Evrard, P. Aimont, X. van der Brempt, J. Jamart, et al., Am. J. Respir. Crit. Care. Med. 151 (1995) 54–60. [9] O. Vandenplas, Eur. Respir. J. 8 (1995) 1957–1965. [10] S.M. Tarlo, L. Wong, J. Roos, N. Booth, J. Allergy Clin. Immunol. 85 (1990) 626–631. [11] G. Pisati, A. Baruffini, F. Bernabeo, P. Falagiani, J. Allergy Clin. Immunol. 101 (1998) 327–329. [12] D. Hadjiliadis, K. Khan, S. Tarlo, J. Allergy Clin. Immunol. 96 (1995) 431–432. [13] S.M. Tarlo, G.L. Sussman, D.L. Holness, J. Allergy Clin. Immunol. 99 (1997) 396–401. [14] D. Levy, S. Allouache, M. Chabane, F. Leynadier, P. Burney, J. Am. Med. Assoc. 281 (1999) 988. [15] D. Gautrin, H. Ghezzo, C. Infante-Rivard, J.-L. Malo, Am. J. Respir. Crit. Care. Med. 162 (2000) 1222–1228. [16] S. Archambault, J.-L. Malo, C. Infanti-Rivard, H. Ghezzo, D. Gautrin, J. Allergy Clin. Immunol. 107 (2001) 921–923. [17] J. Saary, S. Tarlo, A. Kanani, H. Al-Gadeer, D. Holness, J. Allergy, Clin. Immunol. 109 (2002) 131–135. [18] X. Baur, Z. Chen, H. Allmers, J. Allergy Clin. Immunol. 101 (1998) 24–27. [19] X. Baur, Z. Chen, V. Liebers, Clin. Exp. Allergy 28 (1998) 537– 544. [20] D.H. Beezhold, W.C. Beck, Arch. Surg. 127 (1992) 1354–1357. [21] V.J. Tomazic, E.L. Shampaine, A. Lamanna, T.J. Withrow, J. Allergy Clin. Immunol. 93 (1994) 751–758. [22] D.K. Heilman, R.T. Jones, M.C. Swanson, J.W. Yunginger, J. Allergy Clin. Immunol. 98 (1996) 325–330. [23] M.C. Swanson, M.E. Bubak, L.W. Hunt, J.W. Yunginger, M.A. Warner, C.E. Reed, J. Allergy Clin. Immunol. 94 (1994) 445–551. [24] S.M. Tarlo, G.L. Sussman, A. Contala, M.C. Swanson, J. Allergy Clin. Immunol. 93 (1994) 985–989. [25] B.L. Charous, P.J. Scheunemann, M.C. Swanson, Ann. Allergy Asthma Immunol. 85 (2000) 285–290. [26] S. Tarlo, A. Easty, K. Eubanks, C. Parsons, F. Min, S. Juvet, et al., J. Allergy Clin. Immunol. 108 (2001) 628–633.

B.L. Charous et al. / Methods 27 (2002) 15–21 [27] G. Liss, S. Tarlo, Am. J. Ind. Med. 40 (2001) 347–353. [28] C. Blanco, R. Castillo, J. Quiralte, N. Ortega, C. Dominguez, T. Carrillo, Clin. Exp. Allergy 28 (1998) 71–76. [29] D. Ebo, W. Stevens, C. Bridts, L. DeClerck, J. Allergy Clin. Immunol. 100 (1997) 618–623. [30] D. Hadjiliadis, D. Banks, S. Tarlo, J. Allergy Clin. Immunol. 97 (1996) 1202–1206. [31] K.J. Kelly, V. Kurup, M. Zacharisen, A. Resnick, J.N. Fink, J. Allergy Clin. Immunol. 91 (1993) 1140–1145. [32] R. Hamilton, R. Biagini, E. Krieg, J. Allergy Clin. Immunol. 103 (1999) 925–930. [33] H. Yeang, Ann. Allergy Asthma Immunol. 84 (2000) 628–632. [34] O. Vandenplas, F. Binard-Van Cangh, A. Brumagne, J.-M. Caroyer, J. Thimpont, C. Sohy, et al., J. Allergy Clin. Immunol. 107 (2001) 542–547. [35] P. Yellowlees, J. Alpers, J. Bowden, G. Bryant, R. Ruffin, Med. J. Aust. 146 (1987) 305–307. [36] P. Yellowlees, S. Haynes, N. Potts, R. Ruffin, Med. J. Aust. 149 (1988) 246–249. [37] R. Carr, P. Lehrer, S. Hochron, A. Jackson, J. Abnorm. Psychol. 105 (1996) 137–141.

21

[38] P. Lehrer, S. Isenberg, S. Hochron, J. Asthma 30 (1996) 5–21. [39] J. Smoller, M. Pollack, M. Otto, J. Rosenbaum, R. Kradin, Am. J. Respir. Crit. Care. Med. 154 (1996) 6–17. [40] R. Carr, J. Psychosomat. Res. 44 (1998) 43–52. [41] R. Carr, J. Asthma 36 (1999) 143–152. [42] S. Ball, E. Borel, D. Adkins, S. Delaney, Psychosomatics 40 (1999) 135. [43] D. Campbell, R. Sanderson, S. Laverty, J. Abnorm. Social Psychol. 68 (1964) 627–639. [44] G. Davey, Adv. Behav. Res. Ther. 14 (1992) 29–66. [45] M. Primeau, K. Kurt, R. Hamilton, J. Schaefer, J. Adkinson, J. Allergy Clin. Immunol. 104 (2000) S245. [46] D. Shusterman, J. Balmes, J. Cone, J. Occup. Med. 30 (1988) 565– 567. [47] E. McFadden, T. Luparello, H. Lyons, E. Bleecker, Psychosomat. Med. 31 (1969) 134–143. [48] A. Longley, L. Fiset, T. Getz, P. Van Arsdel, P. Weinstein, Gen. Dentistry 42 (1994) 236–240. [49] B.L. Charous, C. Blanco, S. Tarlo, R.G. Hamilton, X. Baur, D. Beezehold, G. Sussman, J.W. Yunginger, J. Allergy Clin. Immunol. 109 (2002) 31–34.