Prevention of Baker’s Asthma

Abstract

Purpose of the review:

Baker’s allergy and asthma continue to represent an important contributor of occupational asthma globally. This review identified recent studies related to the prevention of baker’s allergy and asthma.

Recent findings:

Studies with respect to regulatory exposure standards, workplace control measures aimed at reduction of flour dust exposures, surveillance programmes (exposure monitoring, medical surveillance) and workplace information, education and training programmes were identified.

Summary:

Detailed knowledge on risk factors and detection methods to assess exposure and early identification of high-risk workers exist, but workplace control measures remain sub-optimal since they are rarely multi-faceted. This is compounded by the lack of health-based exposure standards globally. Exposure level monitoring and medical surveillance are integral to assessing effectiveness of preventive strategies. Triage systems for optimising the efficiency of medical surveillance programmes show promise, but need replication in different contexts. Future studies need to focus on evaluating the relevance and quantification of peak exposures in increasing risk; developing standardized respiratory questionnaires for medical surveillance; and further exploration of serial fractional exhaled nitric oxide (FeNO) measurements as an adjunct to allergic sensitization for the early identification of baker’s asthma and assessing the long-term impact of interventions.

INTRODUCTION

Baker’s allergy and asthma remains one of the most common forms of occupational asthma (OA) globally. It is well documented that exposure to flour dust increases the risk of allergic sensitization, rhinitis and asthma in various settings (highly mechanised plants, craft and “in-store supermarket” bakeries). Epidemiological studies report a wide range in the prevalence and incidence of sensitization to wheat flour (5–28%) and 2.2–4.2% per person year (22–42 per 1 000 pyrs), respectively. For fungal α-amylase, the prevalence of sensitization is relatively lower, varying between 2–16%, with an incidence of 2.5% pyr (25 cases per 1 000 pyrs). Occupational rhinitis prevalence is between 18–29% and its incidence ranges between 41–131 per 1000 pyrs. OA prevalence on the other hand, ranges between 4–13%, while incident rates are 3–41 cases per 1 000 pyrs. Prospective studies of young bakers found incidence rates of 29.4 cases per 1 000 pyrs for rhinitis and 0.3–2.4 cases per 1 000 pyrs for OA [1,2]. Despite the long history and persistently high rates of bakers’ asthma, preventive efforts aimed at reducing risks continue to provide disparate and varied results.

The aim of this review was to focus on recent studies on the prevention of baker’s asthma with reference to regulatory frameworks, workplace control measures aimed at reduction of flour dust exposures, surveillance (exposure monitoring, medical surveillance), and workplace education and training programmes.

METHODS

Published studies were identified from PubMed and MEDLINE for the period 2017–19. The following keywords were used in the search strategy: (wheat allergen) OR (flour dust OR wheat allergens) OR (baker’s asthma OR rhinitis) AND occupational exposure) AND (prevention OR intervention OR reduce OR reducing OR reduction). References published within the timeframe not otherwise identified in the initial search were added to provide appropriate continuity and context.

PREVENTION STRATEGIES FOR REDUCING FLOUR-DUST EXPOSURE AND BAKER’S ASTHMA

Different strategies have been identified at various levels (primary, secondary or tertiary), either on its own or in combination with others, to reduce the risk of baker’s allergy and asthma. These strategies are aimed at reducing flour dust exposures, the risk of sensitization, or development of allergic respiratory disease (rhinitis, occupational asthma). Systematic reviews and consensus statements have consistently recommended primary prevention, focused on exposure prevention as the preferred strategy [3].

PRIMARY PREVENTION

Policy, regulatory frameworks and exposure standards

An increasing body of evidence has demonstrated that the risk for allergic sensitization and airway disease increases in a dose dependent manner irrespective of atopic status. Two major approaches have been used to reduce exposure. One, considers flour dust analogous to grain dust and sets a total dust exposure limit at 10 mg/m³ time-weighted average (TWA) and denoting it a sensitiser. However, the high sensitization potential of flour dust makes this standard inadequate in protecting the health of exposed workers since relatively low concentrations increases the risk of allergic respiratory disease [4]. There is therefore a need for specific occupational exposure limits for the main flour dust allergens such as wheat, rye and α-amylase. The American Conference of Government Industrial Hygienists (ACGIH) adopted a threshold limit value (TLV) of 0.5 mg/m³ for flour dust as early as 1999 (Table 1) [5], which were also adopted by the European Union and some countries. Since it was based primarily on health and technical analytical considerations, specific country regulatory standards factored in socio-economic considerations, which resulted in a range between 1–10 mg/m³ being adopted. Compliance with the ACGIH standard has been a challenge. Zamani et al, found that Iranian flour mill workers with mean levels of total dust of 11.06 mg/m³, had almost half (45%) of the samples collected above this standard [6]. Similarly, Canadian bakeries had total dust levels, on average, double the current standard [7]. Norwegian bakeries also reported that 29% of measurements were above its occupational exposure limit (OEL) of 3 mg/m³ [8]. While practicability considerations are important for employers, adopting less conservative standards or employer non-compliance with these standards, has contributed to the disease burden observed.

Table 1.

List of occupational exposure limits (OELs) for flour dust

Substance	OEL (8-h time-weighted average, Total fraction, unless otherwise specified)	Country
Flour dust	0.5 mg/m3	Belgium, Israela, South Koreaa, USA (ACGIH, CAL OSHA), Canada (Alberta)
	1 mg/m3	Ireland, EU (SCOEL)
	2 mg/m3	Finland
	3 mg/m3	Canada (Ontario)a, Sweden, Norwaya
	4 mg/m3	Austria, Spaina
	6 mg/m3	Latvia
	10 mg/m3	UK
	Short term:
	8 mg/m3	Austriab
	30 mg/m3	UKc

^ainhalable fraction,

^b30‐min average,

^c15‐min average

Adapted from Jeebhay et al. [5]

In contrast, the National Health Council in the Netherlands (DECOS) proposed a new health-based recommended OEL (HBROEL) for inhalable wheat flour dust in 2017 addressing respiratory allergic diseases as well as sensitization [9]. This risk evaluation approach, used exposure–response relationships to determine a level associated with an excess risk for wheat sensitization. An excess risk of 1% above the background prevalence of sensitization of 2% in the community was used. A previous recommendation in 1998 proposed an advisory value of 0.12 mg/m³. A reanalysis incorporating data from South Africa and the Netherlands, produced a revised estimate of 0.04mg/³. Since the former population had a higher prevalence of atopy and different working conditions, this estimate was not considered to be generalizable and a revised level of 0.2 mg/m³ was proposed, which produced more stable and reliable estimates than its earlier HBROEL. A similar approach for fungal α-amylase was used and a HBROEL of 0.9 ng/m³ was proposed for all workers irrespective of atopic status [10]. The establishment of evidence-based exposure standards, irrespective of atopic status, represents a major advance for preventative strategies that could further contribute to the reduction of the allergic respiratory disease burden.

While most occupational exposure limits are based on 8-hour time-weighted average exposures, it is increasingly being appreciated that peak exposures associated with very dusty tasks during a working day may indeed play an important role. A few countries have proposed short-term limits to possibly account for peak exposures. However, the basis for the computation of these limits is unclear since current exposure assessment and biostatistical techniques to evaluate peak exposures are not well-developed.

Workplace control measures to reduce flour dust and allergen exposures

Engineering and administrative controls

Control measures aimed at exposure reduction constitute another cornerstone in the prevention of occupational asthma. These primary preventive measures are outlined in Table 2. Since total avoidance is not possible in bakeries, exposure reduction is the preferred approach. Previous studies reported that use of a silo system, enabled closed transmission of flour to the mixer tub, while more recent studies also focus on local exhaust ventilation (LEV), changing and adjusting work practices, appropriate cleaning techniques and the use of respiratory protective equipment (RPE).

Table 2.

Examples of workplace control measures in the primary prevention of baker’s asthma

Level of preventative measure	Type of preventative measure	Workplace sensitizer use or target group	Intervention measure
Substitution (aimed at source)	Substitution/removal	Developing alternatives	Use of divider oil instead of flour for dusting tables
			For enzymes - encapsulated, micro palletized, pastes, liquids or less dusty improver (enzyme) products
Engineering controls (aimed along path)	Ventilation	High-risk workers, bakers	Local exhaust ventilation (LEV) at flour release points (weighing stations dough brakes, bread machines), LEV ring around dough mixer
	Process isolation	All workers	Enclosure of silos (when dumping flour)
	Process modification	All workers	Refitted mixer lids to reduce exposure, automation of dough brakes
Administrative controls (aimed at worker)	Work practice changes	All workers	Use of a sieve for dusting tables, rubbing flour on tables instead of high dusting practices
			Careful bag handling
			Use of vacuum cleaners instead of brooms
	Education and training	All workers	Training on safe work practices
	High-risk individuals focus	Apprentice/trainee programs, asthmatics	Education on work-related asthma, risks and recognition
Personal protective equipment (PPE) (aimed at worker)	Respiratory protective devices (masks)	High-risk workers, dusty tasks (weighing etc.)	Readily available respirators, fit testing, worker education

Framework adapted from Tarlo and Liss (2010)

A strategy used in the UK, focused on changing the physical form of flour improvers as an alternative approach to prevent new cases of sensitization. However, whilst improvers/enzymes are available as pastes or liquid, that are associated with lower exposures, mixing it in a dry powder form was preferred by the industry since it ensured thorough dispersion throughout the flour, but resulted in higher exposures. Mason et al, demonstrated that improver modifications, such as increasing oil content of flour by a small amount, compared to standard improvers or those with reduced calcium silicate or sulphate, significantly decreased dust allergen levels. This may represent a simple, practical method of reducing exposure and could be a useful adjunct to engineering controls, changes to work practices and appropriate training in reducing the risk to bakers’ respiratory health [11].

However, there are few well-designed systematic intervention studies with detailed exposure data to evaluate the effectiveness of exposure reduction approaches. Recently, some new data is emerging on the effectiveness of interventions used in South African supermarket bakeries and the impact on reducing incidence of allergic sensitization [12]. This was part of a larger group randomised study that demonstrated the effectiveness of multi-faceted interventions to reduce exposure to flour dust (and wheat allergen) reporting reductions due to refitting of mixer lids (67%), divider oil (63%) or focused training (54%), with the greatest reduction observed using a combination of control measures (80%) [13]. A recent Norwegian study reported elevated exposures across various bakeries, despite the presence of control measures, concluding that they were ineffective. These were attributed to partial introduction of control measures (local exhaust system or lid on mixer) or suboptimal performance of control measures (mechanical ventilation system, industrial vacuum cleaners) [8].

Information, education and training

As mentioned previously, the Norwegian study found that 29% of measurements exceeded their OEL, despite bakers having knowledge about the harmful health effects of flour dust and a sustained focus by regulatory bodies and the industry on reducing exposure levels [8]. Training on its own does not necessarily prevent injuries and illnesses. It has previously been observed that improvement in workers’ knowledge about the health risks associated with flour-dust exposures, may not necessarily lead to changes in their work practices. Nevertheless, the use of appropriate knowledge and effective dust control measures, coupled with training and supervision, have the potential to reduce exposures in bakeries [13]. In addition to general safety training of all workers, specific education directed at asthmatics on the possible impact of exposures on their asthma may also contribute to improved adherence to appropriate protective measures and improve early reporting for medical assistance. These initiatives could be provided by an occupational health service provider or through web-based information programs, which have been shown to have a positive long-term educational effects [14].

SECONDARY PREVENTION

Exposure level monitoring and surveillance

Exposure assessment is a crucial element in the recognition and management of allergen-related asthma risks, through assessing sources of high-risk exposures and the effectiveness of interventions to reduce dust exposures [10]. A systematic review and meta-analysis on the estimation and validation of flour dust exposure from 21 studies, demonstrated that tasks such as weighing/mixing and dough forming had the highest inhalable dust (3.078–4.930 mg/m³) and wheat allergen levels (37–40 μg/m³) [7]. Multivariate models demonstrated that tasks such as weighing and mixing, dough forming and small bakery size were significant predictors of higher inhalable dust and wheat allergen concentrations.

Kirkeleit et al, demonstrated that extra-thoracic dust particles depositing in the upper airways from a dough mixer, contributed approximately 85% of the inhalable dust composition with an overall exposure level averaging 2.2 mg/m³ [8]. Given the variation in correlations observed between dust fractions across bakery types and task groups in this study, a better understanding is required of how various aerosol fractions are distributed across the production process and bakery types.

Aside from allergens, particle contamination and bioburden from other microbial sources in relation to work-related symptoms has also been highlighted. A newly developed electrostatic dust cloth (EDC) passive sampling device for assessing organic dust exposure in Portuguese bakeries provided important insights [15]. This method allowed for identification of critical worksites in bakeries and was found to be a useful screening and complementary method for assessing bioburden in occupational environments.

Medical surveillance

Medical surveillance aims to detect allergic sensitization and symptoms of rhinitis and asthma at an early stage before the disease becomes severe or irreversible. Surveillance tools have included individual tools or a combination of periodic respiratory questionnaires, spirometry, specific immunologic tests (sIgE, skin prick tests) to common bakery allergens (wheat, rye and α-amylase). More recently tests for airway inflammation (fractional exhaled nitric oxide, sputum eosinophilia, and exhaled breath condensate) have also been used [16]. These tests or components thereof are repeated at different intervals, generally every 6 to 12 months, especially in the first two years, although their ideal frequency is not known [3]. Heightened surveillance (routine 6 monthly) for workers with ‘pre-existing asthma’ or rhinitis is advisable since they are at increased risk of developing occupational asthma.

While respiratory questionnaires are routinely used to record pre-existing and new symptom onset in high-risk workers, generally accepted and validated questionnaires for OA do not exist [3]. Despite variable sensitivity (58–100%) and specificity (45–100%) for early detection of OA, they remain a key component of programmes [16]. The results of immunological testing are more promising following results of a recent review and meta-analysis by Baur et al, which demonstrated a satisfactory performance of sIgE for high molecular weight (HMW) allergens with a pooled sensitivity of 0.74 and specificity of 0.71 [17]. The sensitivity was much higher for wheat (84%) as well as for rye flour (84%). Furthermore, sIgE tests for whole wheat or rye flour extracts had superior diagnostic sensitivity, compared to their allergenic components.

Fractional exhaled nitric oxide (FeNO) has increasingly been used as a complementary tool to spirometry for detecting allergic airway inflammation, due to the easy portability of instruments in the workplace, but its usefulness in screening has been mixed [18]. Beretta et al, demonstrated that 59% of subjects (n=17) with confirmed OA on allergen specific inhalation challenge (SIC) with normal baseline bronchial hyperresponsiveness (BHR) displayed either FeNO ≥25 ppb or sputum eosinophil count ≥2%, concluding that these indices improved the positive identification of subjects with OA [19]. This is consistent with findings from another study that FeNO assessments before and after SIC with occupational agents are highly predictive of OA [20]. Furthermore, serial FeNO assessments during periods away from and at work were found to provide complementary information for diagnosing OA in 20% of workers with suspected disease [21].

There has also been increasing interest in serial measurements of FeNO over longer periods in identifying individuals at higher risk of developing asthma. A study of apprentices (bakers, pastry makers and hairdressers) demonstrated that an increase in FeNO between 6 monthly visits over a 24-month period, rather than elevated FeNO at baseline, predicted the emergence of BHR [22]. However, baseline BHR, was consistently associated with high levels of inflammatory markers and the occurrence of possible asthma.

Given the large numbers of bakery workers in employment in various settings, routine medical assessments may not be feasible or cost-effective. Newer approaches to medical surveillance have been developed in the Netherlands (n=436 bakers), based on diagnostic models using simple short self-administered questionnaires to predict baker’s asthma and rhinitis in workers at high risk of sensitization and requiring further clinical evaluation [23]. Tests for internal validity showed that the models had satisfactory discrimination, but these need to be validated in different populations.

A recent novel study by Taghiakbari et al, using information from clinical interviews, skin-prick test (SPT), spirometry and BHR tests developed non-specific inhalation challenge-based models and clinical scores for diagnosing OA due to high molecular weight agents (53% exposed to flour and associated agents) [24]. The final model, which included age ≤40 years, rhino-conjunctivitis, inhaled corticosteroid use, agent type, non-specific BHR, and work-specific sensitization had a reasonable internal validity. This is a useful approach for resource poor settings without access to SIC to confirm a diagnosis of OA.

Finally, relatively few studies have specifically evaluated the effectiveness of medical surveillance programs. A Finnish record review of patients in surveillance programmes diagnosed with sensitizer-induced OA, found that 18% of cases were detected through surveillance, and only 8% of diagnostic evaluations were initiated by respiratory symptoms [25]. There was a median delay of 2.2 years from onset of asthma symptoms to diagnosis. This is consistent with studies comparing in-house surveillance programmes to those conducted by researchers, which demonstrated that the latter was more accurate (1% vs 4%) in identifying workers with work-related symptoms and flour sIgE tests [16].

In the South African supermarket bakery intervention study, a greater decline in the incidence of cereal flour sensitization (21% versus 6%) and mean FeNO in bakers with baseline FeNO ≥ 25 ppb (16.9 ppb vs 7.7 ppb) was observed in the intervention compared to the control group, one year after the intervention [12]. The study further demonstrated that belonging to the intervention group was a significant predictor of longitudinal decline (≥ 10%) in FeNO over one year. This was particularly evident in bakers with work-related ocular-nasal symptoms at baseline (OR=3.73, CI: 1.22–11.42) using multivariate models that adjusted for smoking status, cereal flour sensitization and elevated baseline FeNO (Al Badri FM, Baatjies R, Jeebhay MF, unpublished data).

TERTIARY PREVENTION

Tertiary prevention is generally focused on optimizing treatment for OA and co-existing rhinitis which is no different to that of allergic asthma of non-occupational causes. Factors associated with improved prognosis include early diagnosis accompanied by removal from exposure, normal or mildly impaired lung function at the time of diagnosis and worker’s compensation support. Previous studies have reported on the possible use of immunotherapy, but these have had mixed results due to the multiple allergens implicated in baker’s asthma.

CONCLUSION

In conclusion, this review has highlighted that baker’s allergy and asthma continue to represent an important entity of OA due to HMW agents. Aside from the need for improved workplace control measures, exposure standards in a number of countries are not totally protective. Despite the existence of detailed knowledge on risk factors and detection methods for identifying those affected at an early stage, few studies exist on the effectiveness of preventive strategies to decrease the disease burden. Future studies need to focus on evaluating the relevance and quantification of peak exposures (as opposed to TWA exposures across the working day); development of standardized respiratory questionnaires for OA/OR surveillance; assessing the effectiveness of triage algorithms for medical surveillance in different geographical contexts; and the utility of serial FeNO measurements as an adjunct to allergic sensitization in the early identification of baker’s asthma and assessing the long-term impact of interventions needs replication in other settings.

Key points.

• Baker’s allergy can be prevented by improved health-based exposure standards

• Multi-faceted workplace control and administrative measures accompanied by education and training can reduce flour dust, allergen exposures and adverse health outcomes

• Exposure level monitoring and medical surveillance are integral to prevention and can be used to assess effectiveness of preventive strategies

• Triage algorithms used in workplace-based medical surveillance provide opportunities for greater efficiency in identifying baker’s allergy and asthma